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Article

Twenty Years of Experience in Juvenile Nasopharyngeal Angiofibroma (JNA) Preoperative Endovascular Embolization: An Effective Procedure with a Low Complications Rate

1
Neuroradiology Unit, ASST Sette Laghi-Circolo Hospital, 21100 Varese, Italy
2
Department of Biotechnology and Life Sciences, Division of Neurosurgery, University of Insubria, 21100 Varese, Italy
3
Department of Biotechnology and Life Sciences, Division of Otorhinolaryngology, University of Insubria, 21100 Varese, Italy
4
Department of Surgical Specialities, Division of Otorhinolaryngology, ASST Sette Laghi-Circolo Hospital, 21100 Varese, Italy
5
Department of Head and Neck Surgery and Otorhinolaryngology, European Institute of Oncology IRCCS, 20122 Milano, Italy
6
Department of Otorhinolaryngology, ASST Lariana, University of Insubria, 22100 Como, Italy
7
Department of Surgery, ASST Lariana, University of Insubria, 22100 Como, Italy
8
Head and Neck Surgery & Forensic Dissection Research Center (HNS&FDRc), Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy
9
Diagnostic and Interventional Neuroradiology Unit, ARNAS Civic Hospital, 90127 Palermo, Italy
10
Radiology Unit, ASST Sette Laghi-Circolo Hospital, 21100 Varese, Italy
*
Author to whom correspondence should be addressed.
J. Clin. Med. 2021, 10(17), 3926; https://doi.org/10.3390/jcm10173926
Submission received: 23 July 2021 / Revised: 20 August 2021 / Accepted: 23 August 2021 / Published: 31 August 2021
(This article belongs to the Special Issue Embolization Techniques: State of the Art and Future Perspectives)

Abstract

:
Juvenile nasopharyngeal angiofibroma (JNA) is a benign tumor of the nasal cavity that predominantly affects young boys. Surgical removal remains the gold standard for the management of this disease. Preoperative intra-arterial embolization (PIAE) is useful for reductions in intraoperative blood loss and surgical complications. In our series of 79 patients who underwent preoperative embolization from 1999 to 2020, demographics, procedural aspects, surgical management and follow-up outcome were analyzed. Embolization was performed in a similar fashion for all patients, with a superselective microcatheterization of external carotid artery (ECA) feeders and an injection of polyvinyl alcohol (PVA) particles, followed, in some cases, by the deployment of coils . Procedural success was reached in 100% of cases, with no complications such as bleeding or thromboembolic occlusion, and surgical intraoperative blood loss was significantly decreased. In conclusion, PIAE is a safe and effective technique in JNA treatment, minimizing intraoperative bleeding.

1. Introduction

Juvenile nasopharyngeal angiofibroma (JNA) is a highly vascularized and histologically benign tumor of the nasal cavity and paranasal sinuses, with aggressive behavior and locally invasive growth patterns [1]. It comprises 0.05% of head and neck tumors and predominantly occurs in young boys, with a mean age of presentation of 15 years [2,3]. The best treatment to date remains surgical removal of the tumor [3]. Preoperative embolization is used for virtually all cases of JNA, resulting in reduction in intraoperative bleeding, occlusion of surgically inaccessible arterial feeding vessels, decreased operative time and improved surgical visualization, identification and protection of adjacent structures [4,5,6]. This results in a significant reduction in overall surgical complications and, despite some reports of safe resection without embolization, it is considered to be the standard of care in most centers [7,8,9]. In this study, we describe our single-center experience in preoperative JNA devascularization with the injection of polyvinyl alcohol (PVA) into major lesion feeders, highlighting the safety and efficacy of this technique. Furthermore, we put emphasis on the detection of external carotid artery (ECA)-internal carotid artery (ICA) anastomoses, defining the main red flags to be considered during preoperative intra-arterial embolization to avoid intraprocedural iatrogenic embolic complications.

2. Materials and Methods

2.1. Data Collection

The study was performed in compliance with the Helsinki Declaration and with policies approved by the Insubria Board of Ethics. All patients involved in the study signed a consent form to publish their clinical photographs whenever useful.
We performed a retrospective analysis of 79 patients treated surgically at our Institution for JNA between 1999 and 2020 who underwent PIAE of ECA branches with the sole usage of PVA. Angiographic patterns, Radkowski stage [10], surgical approach, surgical time, blood loss, age and follow-up imaging were also listed in the database in Appendix A. CT and MRI scans were performed in all patients in order to assess Radkowski stage (Figure 1).
The main outcomes considered were the incidence of complications related to embolization and/or surgery, residual disease rate and intraoperative blood loss.

2.2. Endovascular Embolization

The same approach was performed for every patient, with right groin puncture and placement of 6F femoral sheath, catheterization of internal/external carotid artery (ICA/ECA) and vertebral artery (VA) with angiographic study of their vascular regions (Figure 2), followed by 6F guide catheter (Envoy MPC 90 cm, Cordis) in proximal ECA and superselective catheterization of lesion feeders. Microcatheters used (Rebar 18, Medtronic; SL-10, Stryker) ranged from 0.0165 in to 0.021 in of internal diameters; guidewires used (Traxcess 14, Synchro 10, Synchro 14, Stryker) ranged from 0.010 in to 0.014 in. A control run was then performed from the microcatheter to look for dangerous collaterals and determine the precise position of the distal tip (Figure 3). Embolization was then performed using PVA particles (Contour, Boston Scientific, Marlborough, MA, USA) with different sizes—ranging from 250–355 µm to 500–710 µm—in a slow infusion using blank roadmap visualization to achieve as proper distal penetration as anatomically possible until complete stasis of flow within each feeding vessel was achieved. Adjunctive coil embolization with GDC platinum coil was performed if particle embolization turned out to be incomplete, especially in the case of hypertrophied IMA. At the end of the procedure, control angiography was performed from both ICA and ECA to assess the percentage of tumor feeders embolized. Successful embolization was determined as a lack of contrast in the vascular territory of the embolized vessel (Figure 4).

3. Results

In total, 79 patients were included in this series. The mean age was 18 years (range 10–63 years); all of them were male (100%). The most common symptom was epistaxis (55%), followed by nasal obstruction (50%). According to the classification of Radkowski et al., 3/79 (3.8%) type IA, 7/79 (8.9%) type IB, 26/79 (32.9%) type IIA, 7/79 (8.9%) type IIB, 21/79 (26.6%) type IIIA and 15/79 (18.9%) type IIIB tumors were treated. PIAE with PVA intra-arterial injection was performed in all patients. All cases displayed tumor arterial supply from ECA and/or ICA circulations on 2D angiograms, with a total number of arterial tumor feeders embolized in a given session ranging between 1 and 5.
The technical success of angiography and embolization of almost one big feeder was 100%. Embolization of the JNAs was performed in all cases (79/79) (100%); from distal sphenopalatine branches of the internal maxillary artery in 35/79 cases (44.3%); from ascending pharyngeal artery branches in 20/79 cases (25.3%); from an accessory branch of the middle meningeal artery (MMA) in 7/79 cases (8.9%); from the facial artery and a deep temporal branch of the MMA in 5/79 cases (0.6%); and, in 64/79 cases (81%), procedures were performed under general anesthesia, while the other 15 (18.9%) were performed under conscious sedation.
There was no post-procedural bleeding and there were no thrombo-embolic cerebral ischemic complications in any patient. In no case were there any complications such as vascular dissections, groin hematomas or other complications related to vascular microcatheterization or embolization. Neck pain was experienced by a few patients, and was promptly resolved with analgesic medications. Tumors was removed in all cases within 24 h after embolization. All patients underwent surgery through an endoscopic endonasal approach. All patients were neurologically intact after surgery. Diagnosis of JNA was confirmed histopathologically after surgery.
Follow-up imaging was predominantly performed with MRI. Residual lesions were identified in 7/78 patients (8.9%). In post-surgical remnant JNA patients, the mean size of the preoperative lesion and the presence of vascular afferent from the ICA was greater than in JNAs, in which gross total resection occurred. Of all the post-surgical remnant JNAs, only 2/79 (2.5%) underwent new surgical treatment. Demographic, clinical and surgical data of the 79 patients are summarized in Table 1.

4. Discussion

In this study, we documented an excellent safety profile of PIAE with PVA, reporting no complications directly related to the embolization.
JNA is a rare, benign, vascular lesion of the skull base that affects young adolescent males most commonly between 9 and 19 years of age [3,10]. It is highly aggressive and associated with significant morbidity. Its tendency for skull base erosion, intracranial extension (20% of cases) and high vascularity (vascular component in a fibrous stroma with single endothelial lining) make surgical resection challenging, with a relevant risk for blood loss during resection, post-surgical remnants and lesion recurrence [9].
JNA commonly originates in the posterolateral wall of the nasal cavity, near the superior margin of the sphenopalatine foramen, with progressive diffusion to the anterior nasal cavity, maxillary sinus, pterygoid region, infratemporal fossa and middle cranial fossa [11,12,13]. Signs and symptoms are most often related to tumor extension into the nose, leading to nasal obstruction and epistaxis [10,13,14]. Feeding vessels usually arise from the external carotid system via the internal maxillary artery or ascending pharyngeal artery, but can be highly variable, often with heterogeneous vascularization patterns originating from contralateral ECA, petrous and cavernous branches of ICA, such as mandibulo-vidian artery, inferolateral trunk and ECA-ICA anastomosis, such as ethmoid branches of the ophthalmic artery, which are often related to bigger dimensions [15,16,17].
Traditionally, the open transfacial approach has been the gold standard for JNA excision [1]. In recent years, the advent of endonasal endoscopic approaches (EEAs) has revolutionized the surgical management of these lesions, reducing JNA post-surgical morbidity and recurrence rates [14]. The main advantages of the endoscopic endonasal route are better magnification of the lesion, the dissection of the surgical planes between the lesion and healthy tissue and better cosmetic outcomes. However, JNA resection can still be complicated by massive hemorrhaging because of a rich vascular supply [14,15].
In order to reduce intraoperative bleeding, facilitate surgical lesion removal and improve a patient’s post-operative course, over time, preoperative embolization techniques have been established [18]. The main techniques used for preoperative JNA embolization are endovascular arterial catheterization and direct percutaneous puncture [16,17,18,19].
Pharmacological treatments also have been described to minimize the intraoperative bleeding. Thakar et al. described a significant difference between prepubertal and postpubertal patients in their response to flutamide. Indeed, in postpubertal patients, 6 weeks preoperative may lead to partial tumor regression, facilitating surgical excision and limit morbidity [20].
PIAE is the current most accepted treatment for JNA, minimizing intraoperative bleeding and reducing surgical morbidity [15,17,21,22]. This technique not only reduces the blood supply to the lesion, but the diagnostic preoperative digital subtraction angiography (DSA) highlights the JNA specific vascularization patterns, guiding the surgeon to plan the approach and to delineate lesion areas of increased bleeding risk [15,23]. However, the intra-arterial embolization has some technical limitations, mainly due to the presence of non-embolizable small feeders and to the vascular spasm caused by catheter endovascular manipulation [19]. Furthermore, the presence of ECA-ICA anastomosis directly involved in the vascular supply limits complete JNA devascularization for the risk of inadvertent injection of embolic material into ICA circulation by anterograde crossing from ECA branches through the tumor feeders [16,23,24]. These embolic complications can lead to retinal and cerebral strokes, with iatrogenic blindness and permanent brain damage [24,25,26].
The widely used standard approach for JNA is embolization with particles such as PVA, embospheres (Guerbet Biomedical, Louvres, France) and gelfoam (Upjohn Co., Kalamazoo, MI, USA), all of which have been used successfully for the PIAE of head/neck tumors, as well as in the central nervous system [15,22]. The use of liquid embolic agents (e.g., Onyx), also by percutaneous direct puncture, has been reported to allow for a deeper penetration to tumor capillaries with improved fluoroscopic visibility, as well as a lower risk of catheter adherence [17]. When using PVA, because of its irregular profile (“flakes”), a minimum particle size of more than 150 μm, with a range from 150 to 350 μm, is believed to provide the best compromise between safety (collaterals) and efficient devascularization. As only a temporary occlusion can be achieved, an interval no longer than 7 days between particle embolization and surgery is essential to ensure sufficient devascularization [17,19,27].

5. Conclusions

In this retrospective analysis, PIAE has demonstrated itself to be a safe technique (absence of major intra- or periprocedural hemorrhagic or ischemic complications) and, above all, effective in reducing intraoperative bleeding. Additionally, offering improved intraoperative visibility also reduces postoperative JNA residual rates.

Author Contributions

Conceptualization, A.G., S.M., E.A. and M.B.; methodology, A.G., S.M. and E.A.; software, A.V.T., F.A.V. and A.D.A.; validation, G.P. and L.V.; formal analysis, S.M., E.A., A.D.A., M.T.-Z.; investigation, G.C.; resources, P.C., F.P. and F.M.B.; data curation, S.M.; writing—original draft preparation, S.M. and E.A.; writing—review and editing, A.G., S.M. and E.A.; visualization, A.G., F.M.B. and M.B.; supervision, A.G.; project administration, A.G. and P.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Institutional Review Board (or Ethics Committee) of Insubria Board of Ethics.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

Data are available on request due to restrictions, e.g., privacy or ethical reasons.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table A1. Demographic, procedural, surgical and follow-up data of patients treated in the cohort.
Table A1. Demographic, procedural, surgical and follow-up data of patients treated in the cohort.
Patient No.AgeDate of TreatmentRadkowski StagingSedationSelective EmbolizationAdjunctive CoilsBlood Loss (mL)Embo/Surgery ComplicationsPersistenceSurgery for Recurrence
12020 July 1999IIbGAIMA/APhANo500 NoNoNo
21018 November 1999IaCSIMANo400NoNoNo
3437 May2001IIIaGAIMANo400NoNoNo
41815 May 2001IIaCSIMANo400NoNoNo
51620 February 2002IaGAIMA/APhANo400NoNoNo
61328 February 2002IIIaGAIMA/APhA/FANo650NoNoNo
7173 June 2002IIaCSIMANo200NoNoNo
81429 August 2002IIIbGAIMA/APhANo2800NoYes (CS)No
93112 November 2002IIIaCSIMANo200NoNoNo
101928 January 2003IIaGAIMANo400NoNoNo
111612 March 2003IIIbGAIMA/APhANo1500NoNoNo
121219 February 2004IIIbGAIMA/APhA/AM/DTYes800NoYes (CS)Yes (6/12/2005)
13122 February 2005IIaGAIMANo450NoNoNo
144914 February 2005IIaGAIMA/APhANo200NoNoNo
151621 February 2005IaCSIMANo300NoNoNo
16131 March 2005IIIaGAIMANo700NoYes (PPF)No
171014 March 2005IIIaGAIMA/APhA/AMNo1400NoNoNo
182913 June 2005IIIaCSIMANo500NoNoNo
19365 September 2005IIIbGAIMA/APhA/FAYes2500NoYes (CS)No
201529 November 2005IIIbGAIMA/APhA/AMNo1800NoYes (CS)No
211224 January 2006IIIaGAIMANo800NoNoNo
22199 March 2006IIaCSIMANo200NoNoNo
231314 December 2006IIaGAIMA/APhANo1500NoNoNo
241318 June 2007IIIaGAIMANo350NoNoNo
251528 June 2007IIIaGAIMA/AMNo500NoNoNo
261712 July 2007IIaGAIMANo200NoNoNo
271423 October 2007IIIbGAIMA/APhA/FAYes600NoNoNo
281511 June 2008IIIbGAIMA/APhA/AMNo700NoNoNo
293930 June 2008IIIbCSIMANo200NoNoNo
302022 July 2008IIIbGAIMA/APhA/DTNo5200NoNoNo
31209 September 2008IIIbGAIMA/AMNo300NoNoNo
321430 September 2008IIIaCSIMANo300NoNoNo
331411 November 2008IIaGAIMA/APhA/FANo300NoNoNo
34212 December 2008IIbGAIMA/AMNo700NoNoNo
351817 February 2009IIbCSIMANo1200NoNoNo
362616 June 2009IIIaGAIMA/APhA/DTNo600NoNoNo
371321 January 2010IIIaGAIMA/APhA/AMNo1000NoNoNo
381825 March 2010IIbGAIMANo800NoNoNo
391311 May 2010IIaGAIMANo300NoNoNo
40182 June 2010IIaGAIMA/APhANo100NoNoNo
41209 November 2010IIaGAIMANo1500NoNoNo
421629 November 2011IIbGAIMA/APhANo550NoNoNo
431517 April 2012IbGAIMA/AMNo250NoNoNo
441322 May 2012IIIaGAIMA/APhAYes600NoNoNo
452019 June 2012IIaCSIMANo100NoNoNo
461426 July 2012IIIaGAIMA/APhA/AMNo800NoNoNo
471923 August 2012IIaGAIMANo600NoNoNo
48174 September 2012IIaGAIMANo400NoNoNo
491916 October 2012IIIaGAIMA/AMYes400NoNoNo
50198 January 2013IIaGAIMANo300NoNoNo
511314 May 2013IIIaGAIMA/APhA/AMNo200NoNoNo
521319 June 2013IbGAIMANo500NoNoNo
531320 June 2013IIIaGAIMANo2000NoNoNo
546324 June 2013IIaGAIMANo500Post-surgical bleedingNoNo
551125 June 2013IIIbGAIMA/APhANo1200NoYes (CS)No
561327 August 2013IIaGAIMANo800NoNoNo
572016 January 2014IIaGAIMA/AMNo250NoNoNo
58162 April 2014IIaGAIMANo40NoNoNo
591629 September 2014IIIaGAIMANo450NoNoNo
601512 November 2014IIIbGAIMA/APhA/AMNo1750NoYes (MCF)No
611225 February 2015IIIbGAIMANo2000NoNoNo
621511 March 2015IIIbGAIMA/APhA/AMNo2100NoNoNo
631815 July 2015IIIaGAIMA/APhA/AM/DT/FANo1500NoNoNo
643520 January 2016IIIaGAIMA/APhA/DT/FANo1000NoNoNo
651331 August 2016IIbGAIMA/APhA/AMNo500NoNoNo
661222 September 2016IbGAIMA/APhA/AMNo150NoNoNo
67167 June 2017IIaCSIMANo200NoNoNo
681619 July 2017IIIaGAIMA/APhA/AMYes2500NoNoNo
691319 October 2017IIaGAIMA/APhANo150NoNoNo
701423 January 2018IbGAIMA/APhA/AMYes200NoNoNo
711910 July 2018IbCSIMANo100NoNoNo
721616 August 2018IbCSIMANo50NoNoNo
731218 February 2019IIbGAIMANo150NoNoNo
741526 June 2019IIaGAIMA/APhANo500NoNoNo
751426 September 2019IIbCSIMANo300NoNoNo
761828 November 2019IIbGAIMANo100NoNoNo
772019 December 2019IIaGAIMANo400NoNoNo
78154 May 2020IIaGAIMA/APhA/FANo2000NoNoNo
791330 November 2020IIIbGAIMA/APhANo2500NoNoNo
CS: cavernous sinus; PPF: pterygopalatine fossa; MCF: middle cranial fossa; GA: general anesthesia; CS: conscious sedation; IMA: internal maxillary artery; APhA: ascending pharyngeal artery; DT: deep temporal branch of MMA; AM: accessory meningeal branch of MMA; FA: facial artery.

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Figure 1. Preprocedural MRI scan (Gd-enhanced T1 Gradient-Echo 3D): coronal (a) and axial (b) views showing large JNA of right nasopharyngeal mass with expansion of the pterygopalatine fossa and extension into the infratemporal fossa.
Figure 1. Preprocedural MRI scan (Gd-enhanced T1 Gradient-Echo 3D): coronal (a) and axial (b) views showing large JNA of right nasopharyngeal mass with expansion of the pterygopalatine fossa and extension into the infratemporal fossa.
Jcm 10 03926 g001
Figure 2. Preoperative DSA: selective catheterization of proximal ECA. Posteroanterior (PA) (a) and laterolateral (LL) (b) views of the JNA with major feeders from sphenopalatine branches of the distal internal maxillary artery (IMA) and from the ascending pharyngeal artery (APhA).
Figure 2. Preoperative DSA: selective catheterization of proximal ECA. Posteroanterior (PA) (a) and laterolateral (LL) (b) views of the JNA with major feeders from sphenopalatine branches of the distal internal maxillary artery (IMA) and from the ascending pharyngeal artery (APhA).
Jcm 10 03926 g002
Figure 3. Intraprocedural DSA: PA view of superselective injection of distal IMA (a) and APhA (b) feeders.
Figure 3. Intraprocedural DSA: PA view of superselective injection of distal IMA (a) and APhA (b) feeders.
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Figure 4. Postprocedural DSA: PA (a) and LL (b) views of the JNA showing successful embolization of the lesion.
Figure 4. Postprocedural DSA: PA (a) and LL (b) views of the JNA showing successful embolization of the lesion.
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Table 1. Demographic, clinical and procedural characteristics of the 79 patients.
Table 1. Demographic, clinical and procedural characteristics of the 79 patients.
Variables Data
Age (years)Mean18
Median20
Range10–63
SymptomsEpistaxis55%
Nasal obstruction50%
Rhinolalia14%
Headache12%
Proptosis10%
Diplopia6%
Decreased visual acuity2%
Radkowski classificationType IA4%
Type IB9%
Type IIA33%
Type IIB9%
Type IIIA26%
Type IIIB19%
Intraoperative blood loss (mL)Mean784
Range40–5200
Surgical time (min)Mean217
Range95–625
Neuroimaging follow up (months)Mean25
Median12
Range1–127
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Giorgianni, A.; Molinaro, S.; Agosti, E.; Terrana, A.V.; Vizzari, F.A.; Arosio, A.D.; Pietrobon, G.; Volpi, L.; Turri-Zanoni, M.; Craparo, G.; et al. Twenty Years of Experience in Juvenile Nasopharyngeal Angiofibroma (JNA) Preoperative Endovascular Embolization: An Effective Procedure with a Low Complications Rate. J. Clin. Med. 2021, 10, 3926. https://doi.org/10.3390/jcm10173926

AMA Style

Giorgianni A, Molinaro S, Agosti E, Terrana AV, Vizzari FA, Arosio AD, Pietrobon G, Volpi L, Turri-Zanoni M, Craparo G, et al. Twenty Years of Experience in Juvenile Nasopharyngeal Angiofibroma (JNA) Preoperative Endovascular Embolization: An Effective Procedure with a Low Complications Rate. Journal of Clinical Medicine. 2021; 10(17):3926. https://doi.org/10.3390/jcm10173926

Chicago/Turabian Style

Giorgianni, Andrea, Stefano Molinaro, Edoardo Agosti, Alberto Vito Terrana, Francesco Alberto Vizzari, Alberto Daniele Arosio, Giacomo Pietrobon, Luca Volpi, Mario Turri-Zanoni, Giuseppe Craparo, and et al. 2021. "Twenty Years of Experience in Juvenile Nasopharyngeal Angiofibroma (JNA) Preoperative Endovascular Embolization: An Effective Procedure with a Low Complications Rate" Journal of Clinical Medicine 10, no. 17: 3926. https://doi.org/10.3390/jcm10173926

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