Mucocele formation after surgical treatment of inverted papilloma of the frontal sinus drainage pathway Benjamin Verillaud, M.D., Ph.D.,1 Nicolas Le Clerc, M.D.,1, Jean-Philippe Blancal, M.D.,1 Jean-Pierre Guichard, M.D.,2 Romain Kania, M.D., Ph.D.,1 Marion Classe, M.D.,3, and Philippe Herman, M.D., Ph.D.1

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ABSTRACT

Background: Inverted papillomas (IP) inserted in the frontal sinus and/or recess may be treated by using an endoscopic endonasal or an external approach. There are still few data available on this uncommon localization of IPs. Objective: To report our experience in the management of IP of the frontal drainage pathway, to describe a previously unreported specific complication of this surgery, and to discuss the optimal surgical strategy. Methods: A retrospective study of the patients at a tertiary care center between 2004 and 2014 who were operated on for an IP with an insertion in the frontal recess and/or the frontal sinus. Clinical charts were reviewed for demographics, clinical presentation, imaging findings, surgical treatment, and outcome. Results: Twenty-seven patients were included. Patients were operated on by using a purely endoscopic approach (Draf procedure; n ⫽ 14 [51.9%]) when the IP was inserted in the frontal recess and/or the frontal sinus infundibulum (with a nasoseptal-septoturbinal flap placed on the exposed bone in four patients), or by using a combined endoscopic and open approach (osteoplastic flap procedure; n ⫽ 13 [48.1%]) when the IP invaded the frontal sinus beyond the infundibulum. There were two recurrences (7.4%), with a mean follow-up of 40 months (range, 9 –123 months). During follow-up, single or multiple iatrogenic frontal mucoceles were observed in 10 patients (37%), with a mean delay of 60 months (range, 27– 89 months). These mucoceles occurred both after using endoscopic (n ⫽ 3) or combined (n ⫽ 7) approaches, and required a surgical treatment in eight patients. No postoperative mucocele was observed in the four patients who had had a septal flap. Conclusion: In our experience, an approach based on the localization of the IP insertion provided acceptable results in terms of the local control rate (92.6%). However, the significant rate of postoperative mucoceles indicated that specific strategies (such as local flaps) still need to be developed to avoid this iatrogenic complication. (Am J Rhinol Allergy 30, e181–e184, 2016; doi: 10.2500/ajra.2016.30.4351)

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nverted papillomas (IP) are benign tumors of the nasal cavity. They have a locally destructive behavior and may degenerate into squamous cell carcinoma in 1 to 5% of patients.1,2 Most IPs arise from the lateral wall of the nasal cavity and invade the maxillary sinus or the ethmoid sinus.3 Frontal and sphenoid localizations are rare and account for ⬍10% of cases.1,4 The treatment relies on surgical excision of the tumor, with subperiosteal dissection of the pedicled part of the tumor, and drilling of the underlying bone. Many reports over the past 20 years have led to the consensual conclusion that the endoscopic approach is safe and effective provided that the pedicle of the IP could be fully visualized and controlled.5–7 The improvements in endoscopic techniques as well as in instrumentation now allow better access to the frontal sinus, and several articles have described endoscopic approaches to IPs of the frontal sinus.1,8–10 However, there are still relatively few data on the management of IPs that invade the frontal drainage pathway. The aim of this study was to critically analyze the results of surgical treatment of IPs that involve the frontal sinus, based on a series of 27 patients with prolonged follow-up. We described a previously unreported complication of frontal sinus IP surgery, viz., a significant rate of iatrogenic frontal mucoceles, which should, in our opinion, be taken into account in the choice of a surgical strategy.

From the 1Department of Otorhinolaryngology—Head and Neck Surgery, Lariboisie`re Hospital, Assistance Publique - Hôpitaux de Paris (APHP), Paris VII University, Paris, France, 2Department of Neuroradiology, Lariboisie`re Hospital, APHP, Paris, France, and 3Department of Pathology, Lariboisie`re Hospital, APHP, Paris VII University, Paris, France No external funding sources reported The authors have no conflicts of interest to declare pertaining to this article Address correspondence to Benjamin Verillaud, M.D., Hôpital Lariboisière, 2 rue Ambroise Paré, 75010 Paris, France E-mail address: [email protected] Copyright © 2016, OceanSide Publications, Inc., U.S.A.

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METHODS We performed a retrospective chart review of patients treated between 2004 and 2014 at a tertiary care center for IPs that involved the frontal sinus drainage pathway, i.e., with an insertion into the frontal sinus or into the frontal recess with tumor herniation into the frontal sinus. All the patients underwent clinical examination with nasal endoscopy and preoperative biopsy when the lesion was accessible; computed tomography (CT); and magnetic resonance imaging (MRI) with at least T1, T2, and T1 with gadolinium-weighted sequences. The surgical strategy was based on the tumor location: a purely endoscopic approach was performed when the IP was inserted into the frontal recess and/or the frontal sinus infundibulum, and a combined approach with both an endoscopic and an open approach with osteoplastic flap procedure was used when the IP invaded the frontal recess and the frontal sinus beyond the infundibulum. In case of recurrent IP with invasion of the frontal sinus beyond the infundibulum, a combined approach was always performed, even if the tumor spared the frontal recess so as to clear all the scar tissue within the frontal recess. In all the patients, the frontal drainage pathway was enlarged to maintain the patency of the nasofrontal tract at the end of the procedure. After the early postoperative period, follow-up was based on nasal examination and MRI at 3 months after surgery and then annually. The medical files were reviewed for demographics, history of IP, clinical and radiologic presentation, surgical treatment, and long-term outcome. The present study was approved by the local institutional review board (Comite´ Ethique et de Protection des Personnes Ile de France IV, Hoˆpital Saint-Louis—Lariboisie`re-Fernand Widal), and written consent was obtained from all the patients. Statistical analyses were performed by using R statistical software. We used the Fisher’s exact test for qualitative data and the Student’s t-test for quantitative data. A difference was considered statistically significant if the p value was ⬍0.05.

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Table 1 Inverted papilloma of the frontal sinus drainage pathway: Clinical features, site of insertion, surgical technique, and outcome Patient No.

Age, y

Sex

Previous Surgery

Presenting Signs

1* 2* 3 4* 5 6 7* 8* 9* 10 11 12* 13 14* 15 16* 17 18 19 20 21 22 23 24* 25 26 27

46 51 77 46 71 53 26 53 80 82 79 63 57 31 61 49 55 57 76 67 73 55 80 63 63 63 45

M M M F F F M M M M F F F M M M M M F M M M F M F M M

No Yes No No Yes No Yes No Yes No Yes No No Yes Yes Yes Yes Yes No Yes Yes No Yes No No Yes No

Ptosis Proptosis No symptom Acute frontal sinusitis Follow-up imaging Nasal blockage Nasal blockage No symptom Nasal blockage Nasal blockage Ptosis ⫹ diplopia Nasal deformation Headache Nasal blockage Follow-up imaging Nasal blockage Follow-up imaging Follow-up imaging Nasal blockage Follow-up imaging Follow-up imaging Nasal blockage Proptosis Nasal blockage Nasal blockage Nasal blockage Acute frontal sinusitis

Site of Insertion FR FS FR FR FR FR FR FR FR FR FR FR FR FR FR FR FR FR FR FS FR FR FR FR FR FR FR

⫹ FI ⫹ FS ⫹ FI ⫹ FS ⫹ FI ⫹ FS ⫹ FI ⫹ FI ⫹ FS ⫹ FI ⫹ FS ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹

FI FI FI FI FI FI FI FI FI

⫹ FS ⫹ FS ⫹ FS

⫹ FS

⫹ FI ⫹ ⫹ ⫹ ⫹ ⫹

FI ⫹ FS FI ⫹ FS FI FI FI

T

Type of Approach

Recurrence

Follow-up, mo

Combined approach Combined approach Combined approach Combined approach Draf 2b Draf 1 Combined approach Draf 2b Combined approach Draf 1 Combined approach Combined approach Combined approach Draf 2b Draf 2b Draf 2b Draf 2b ⫹ flap Combined approach Draf 2b ⫹ flap Combined approach Draf 2b Draf 2a Combined approach Combined approach Draf 3 ⫹ flap Draf 2b Draf 2b ⫹ flap

Yes (96 mo) Yes (24 mo) No No No No No No No No No No No No No No No No No No No No No No No No No

112 123 39 109 24 9 86 48 10 13 91 45 34 74 43 27 31 24 24 30 17 9 23 14 10 10 11

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FR ⫽ Frontal recess; FI ⫽ frontal sinus infundibulum; FS ⫽ frontal sinus beyond the infundibulum. *Patients who developed a postoperative mucocele.

RESULTS

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Between 2004 and 2014, 27 patients (17 men and 10 women) were treated surgically for an IP that invaded the frontal sinus drainage pathway. The main clinical features are summarized in Table 1. The mean age at diagnosis was 58 years (range, 26–82 years). Thirteen patients (48%) had been operated on before, all by an endoscopic approach. Presenting signs included nasal blockage (n ⫽ 11 [40%]), orbital signs (ptosis, proptosis, and/or diplopia) (n ⫽ 4 [14.8%]), acute frontal sinusitis (n ⫽ 2 [7.4%]), headache (n ⫽ 1 [3.7%]), and nasal deformation (n ⫽ 1 [3.7%]). Two patients (7.4%) had no symptoms at presentation, and the IP was discovered fortuitously on imaging. In all the other patients, IP was a recurrence discovered on follow-up imaging. Preoperative nasal endoscopy showed a polypoid lesion that originated from the middle meatus in 25 cases (92.6%), but, in two patients with recurrent IP (7.4%), the tumor was located within the frontal sinus and detected only on MRI. The identification of the extension of the IP and of its attachment site was based on the analysis of the CT, which showed a soft-tissuedensity mass with calcification and focal hyperostosis next to the pedicle of the IP, and of the MRI, which helped make the difference between the IP (with a convoluted cerebriform pattern on both T2and contrast-enhanced T1-weighted images) and sinus retention. In all the patients, the definitive identification of the site of insertion of the IP was determined during surgery: it involved the frontal recess in 25 patients (92.6%), with an extension to the frontal infundibulum in 10 patients (37%), and to the frontal sinus beyond the infundibulum in 11 patients (40.7%). Two patients (7.4%) presented with a tumor recurrence located strictly within the frontal sinus. The patients were operated on by using a purely endoscopic approach (n ⫽ 14 [51.9%]) or a combined approach (n ⫽ 13 [48.1%]),

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depending on the location of the IP (as described in the Methods section). Of note, even if the surgical approach was decided before surgery based on the analysis of CT and/or MRI, the patients were informed that the type of approach could be modified, depending on the intraoperative findings; however, no conversion from the endoscopic to the combined approach was necessary in this series. Among the patients operated on through an endoscopic approach, 2 required a Draf type 1 procedure (7.4%), 1 required a Draf type 2a (3.7%), 10 required a Draf type 2b (37%), and 1 required a Draf type 3 (3.7%). In both endoscopic and external approaches, the lesion was fully removed, the site of insertion of the IP was dissected in a subperiosteal plane, and the underlying bone was drilled. The mucosa of the frontal sinus drainage pathway, therefore, was partially or totally removed in all the patients, and, except for the two patients operated on with a Draf type 1 procedure, the floor of the frontal sinus was drilled out to try and maintain a maximal patency of the nasofrontal tract. A local mucosal flap (septoturbinal or nasoseptal flap) was used in four patients who had purely endoscopic procedures (14.8%). Pathologic examinations confirmed the diagnosis of IP in all the patients and revealed a malignant transformation in two patients (7.4%). One of these two patients received adjuvant radiotherapy. There were two recurrences of IP (7.4%), with a mean follow-up of 40 months (range, 9–123 months). During the follow-up, single or multiple iatrogenic frontal mucoceles were observed in 10 patients (37%) and required surgical treatment in 8 patients, with a mean delay of 60 months (range, 27–89 month). Of these 10 patients, 3 had been operated on for their IP by using an endoscopic approach (IP inserted in the frontal recess and/or frontal sinus infundibulum) and 7 by using a combined

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Table 2 Postoperative mucoceles: Clinical features, surgical treatment, and postoperative follow-up (no recurrence to date) Patient No. 1 2 4 7 8 9 12 14 16 24

Type of Approach of the i.p. Combined Combined Combined Combined Draf 2b Combined Combined Draf 2b Draf 2b Combined

approach approach approach approach approach approach

approach

Time of Onset

Symptoms

87 84 89 56 36 10 44 60 26 14

Ptosis Bony erosion Bony erosion Bony erosion Headaches No symptoms Bony erosion Bony erosion Bony erosion No symptom

Surgical Treatment Frontal Frontal Frontal Frontal Draf 3 No Frontal Draf 3 Draf 3 No

sinus sinus sinus sinus

Follow-up, mo

exclusion exclusion exclusion exclusion

Y P

sinus exclusion

i.p. ⫽ Inverted papilloma.

approach (IP inserted in the frontal sinus beyond the infundibulum): the mucocele rate among the patients operated on by using an endoscopic approach and by using a combined approach, therefore, was 21% and 54%, respectively. Statistical analysis revealed that this difference was not significant (p ⫽ 0.12). To explore if the mucocele rate was associated with the size of the frontal sinusotomy rather than to the approach, we measured the size of the opening in the floor of the frontal sinus on postoperative imaging: it was not statistically different in the group of patients who developed a mucocele (average size, 146.8 mm2) and in the other group (151.5 mm2) (p ⫽ 0.87). None of the four patients who had been operated on by using an endoscopic approach with a local mucosal flap developed a frontal mucocele, with a mean follow-up of 19 months (range, 10–31 months). However, once again, there was no statistical difference in the rate of postoperative mucocele between patients operated on with or without a local flap (p ⫽ 0.5). Surgical treatment of the mucoceles was advocated in cases of progressive expansion with erosion of the anterior and/or posterior wall of the frontal sinus (n ⫽ 6), ptosis (n ⫽ 1), or headaches (n ⫽ 1). An external approach with osteoplastic flap and sinus exclusion was performed in five patients, and a Draf type 3 procedure was performed in three patients. Symptoms and surgical outcomes are summarized in Table 2. There were no short-term complications and no recurrence, with a mean follow-up of 18 months (range, 1–39 months).

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DISCUSSION

In this article, we described our experience with the surgical management of IPs that involved the frontal sinus drainage pathway. Traditionally, IPs were removed by using an open approach; however, to our knowledge, there is no specific report of the results of the open approach for IPs of the frontal sinus drainage pathway. Over the past 10 years, several articles have described a purely endoscopic approach of IPs of the frontal sinus by using Draf type 1, 2, or 3 frontal sinusotomy.1,8–10 Lombardi et al.1 described their experience with 212 patients with sinonasal IP, with an insertion in the frontal sinus in 11 patients. A combined approach was performed in 5 of these 11 patients.1 The global recurrence rate was 5.7%, with a mean follow-up of 53.8 months, but 2 of 11 (18%) of the patients with an IP insertion in the frontal sinus experienced IP recurrence; 4 of 212 patients developed a postoperative frontal mucocele.1 However, the specific mucocele rate and follow-up of patients with an IP inserted in the frontal sinus was not specified in this large series.1 Zhang et al.8 reported no recurrence and no complications after purely endoscopic management of nine patients with IP of the frontal sinus or of the frontal sinus drainage pathway (mean follow-up, 15 months). In a retrospective series of 18 patients with frontal sinus IP, Yoon et al.9 reported a recurrence rate of 22% and two intraoperative cerebrospinal fluid leaks that were successfully managed endoscopi-

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cally (mean follow-up, 36 months). Adriaensen et al.10 treated 20 patients with IP that involved the frontal sinus drainage pathway bu using a purely endoscopic approach, and application of 5-fluorouracil in eight patients with recurrence; the overall recurrence rate was 10%, with no recurrence in the patients treated with 5-fluorouracil (mean follow-up, 42 months). In our study, the type of approach depended on the location of the IP, viz., on the involvement of the frontal recess, the frontal infundibulum, and/or the rest of the frontal sinus. Indeed, an adequate control of the site of insertion of the IP seemed to be the key point to prevent recurrence.4 In our opinion, the purely endoscopic approach should be chosen only if the tumor pedicle is limited to the frontal recess and/or the frontal sinus infundibulum. In all the other cases, a combined approach provided an excellent view on the superior and lateral aspects of the frontal sinus but also on the anterior ethmoid and especially the frontal recess.11 As pointed in the Results section, the control of the anterior ethmoid is mandatory because a primary involvement of the frontal recess was observed in almost all the patients: only 2 of 27 patients presented with a recurrence located exclusively within the frontal sinus. With this strategy, we reported acceptable results in terms of local control, with a recurrence rate of 7.4% after a mean follow-up of 40 months. However, there was a significant rate of secondary stenosis of the nasofrontal tract, with subsequent formation of mucocele that required surgical treatment in almost one-third of the patients (8/27). Although the figures were too low to draw general conclusions, an insertion of the IP within the frontal sinus that requires a combined approach may be a predictor for mucocele formation: indeed, most of the patients with mucocele had been operated on by using an open approach. A possible explanation would be that the removal of large areas of mucosa followed by the drilling of the underlying bone results in extended neoosteogenesis along the frontal sinus drainage pathway and subsequent mucocele formation. This theory would also explain the higher rate of iatrogenic mucocele in IP surgery (with drilling of the pedicle site) than in other sinus surgeries.12 This observation led to several conclusions. First, patients should be informed of the risk of long-term complications and followed up long enough to detect these mucoceles.13 Second, a specific strategy should be developed to prevent mucocele formation. One possible strategy would be to systematically discuss frontal sinus exclusion for all patients who present with an IP that invaded the frontal sinus. We chose another strategy. For four of the last patients of our series, we successfully used local flaps to cover the exposed bone after drilling the floor of the frontal sinus. Indeed, local flaps seem to be effective to prevent stenosis of narrow corridors, in frontal sinus surgery but also in other types of surgery, e.g., in the drainage of cholesterol granulomas of the petrous apex.14–16 A longer follow-up, however, will be needed to validate the long-term results of this technique.

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5.

Indeed, the mean time of onset of postoperative mucoceles was 60 months in our series, and the mean follow-up of the four patients operated on with a local flap was only 19 months.

6. 7.

CONCLUSION In this series, we reported a local control rate of 92.6% for IPs with an insertion on the frontal sinus drainage pathway by using the following strategy: IPs with an insertion limited to the frontal recess and/or the frontal sinus infundibulum were removed by using a purely endoscopic approach with a Draf type 1, 2, or 3 procedure, and IPs with an insertion in the frontal sinus beyond the infundibulum were treated by using a combined transnasal-external approach. An interesting finding of this study was the high rate of postoperative mucocele; specific strategies remain to be developed to avoid this iatrogenic complication.

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REFERENCES 1.

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Lombardi D, Tomenzoli D, Butta` L, et al. Limitations and complications of endoscopic surgery for treatment for sinonasal inverted papilloma: A reassessment after 212 cases. Head Neck 33:1154–1161, 2011. Mirza S, Bradley PJ, Acharya A, et al. Sinonasal inverted papillomas: Recurrence, and synchronous and metachronous malignancy. J Laryngol Otol 121:857–864, 2007. Hong SL, Mun SJ, Cho KS, and Roh HJ. Inverted papilloma of the maxillary sinus: Surgical approach and long-term results. Am J Rhinol Allergy 29:441–444, 2015. Lawson W, and Patel ZM. The evolution of management for inverted papilloma: An analysis of 200 cases. Otolaryngol Head Neck Surg 140:330–335, 2009.

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Lund VJ, Stammberger H, Nicolai P, et al. European position paper on endoscopic management of tumours of the nose, paranasal sinuses and skull base. Rhinol Suppl (22):1–143, 2010. Healy DY Jr, Chhabra N, Metson R, et al. Surgical risk factors for recurrence of inverted papilloma. Laryngoscope 126:796–801, 2016. Pagella F, Pusateri A, Giourgos G, et al. Evolution in the treatment of sinonasal inverted papilloma: Pedicle-oriented endoscopic surgery. Am J Rhinol Allergy 28:75–81, 2014. Zhang L, Han D, Wang C, et al. Endoscopic management of the inverted papilloma with attachment to the frontal sinus drainage pathway. Acta Otolaryngol 128:561–568, 2008. Yoon BN, Batra PS, Citardi MJ, and Roh HJ. Frontal sinus inverted papilloma: Surgical strategy based on the site of attachment. Am J Rhinol Allergy 23:337–341, 2009. Adriaensen GF, van der Hout MW, Reinartz SM, et al. Endoscopic treatment of inverted papilloma attached in the frontal sinus/recess. Rhinology 53:317–324, 2015. Carta F, Verillaud B, and Herman P. Role of endoscopic approach in the management of inverted papilloma. Curr Opin Otolaryngol Head Neck Surg 19:21–24, 2011. Suzuki S, Yasunaga H, Matsui H, et al. Complication rates after functional endoscopic sinus surgery: Analysis of 50,734 Japanese patients. Laryngoscope 125:1785–1791, 2015. Scangas GA, Gudis DA, and Kennedy DW. The natural history and clinical characteristics of paranasal sinus mucoceles: A clinical review. Int Forum Allergy Rhinol 3:712–717, 2013. Wei CC, and Sama A. What is the evidence for the use of mucosal flaps in Draf III procedures? Curr Opin Otolaryngol Head Neck Surg 22:63–67, 2014. Karligkiotis A, Bignami M, Terranova P, et al. Use of the pedicled nasoseptal flap in the endoscopic management of cholesterol granulomas of the petrous apex. Int Forum Allergy Rhinol 5:747–753, 2015. Fiorini FR, Nogueira C, Verillaud B, et al. Value of septoturbinal flap in the frontal sinus drill-out type IIb according to draf. Laryngoscope 2016. (Epub ahead of print March 12, 2016.) e

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Mucocele formation after surgical treatment of inverted papilloma of the frontal sinus drainage pathway.

Inverted papillomas (IP) inserted in the frontal sinus and/or recess may be treated by using an endoscopic endonasal or an external approach. There ar...
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