Abstract
The nasopharynx represents an intersection between the nasal choanae, the oropharynx, the deep facial spaces, the skull base and the intracranial cavity. Most nasopharyngeal neoplasms are malignant tumors showing aggressive local infiltration along well-defined routes. The primary role of imaging is accurate tumor mapping and detection of possible tumor extension, especially to the skull base and the deep facial spaces. The aim of this paper is to illustrate these extension patterns of nasopharyngeal carcinomas on imaging and to show the particular implication of imaging in the correct staging of the lesion.
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Introduction
The nasopharynx constitutes the upper part of the pharynx and aerodigestive tract. It lies under the skull base and represents an intersection between the nasal choanae, the oropharynx, the deep facial spaces, the skull base and the intracranial cavity. Most nasopharyngeal neoplasms are malignant tumors. It is fundamental to analyze the extension of these tumors in this area, especially at the skull base foramen and the deep facial spaces.
Specific anatomy
The nasopharynx (Fig. 1) is a cuboid cavity underneath the skull base. The boundaries of the nasopharynx are as follows: superiorly, the basisphenoid and the clivus; posteriorly, the retropharyngeal and prevertebral space; anteriorly, the nasal choanae; inferiorly, the oropharynx; laterally, the parapharyngeal space. Anteriorly, the soft palate separates the nasopharynx from the oropharynx (the posterior side of the soft palate belongs to the nasopharynx, the inferior side to the oropharynx). Posteriorly, there is no clear separation between the nasopharynx and oropharynx; on imaging studies, this separation can be made by drawing a horizontal line along the superior edge of the anterior arch of C1 [1] or through the atlanto-axial articulation, depending on the author.
The nasopharyngeal mucosa consists of epithelium delineating the pharyngeal mucosal space. The sub-mucosal space also contains lymphoid tissue, accessory salivary glands, cellular notochord remnants, and tensor and levator veli palatini muscles. There are two main mucosal-lined recesses (Fig. 2):
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the eustachian tube orifice, just in front of the torus tubarius
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the lateral pharyngeal recess or fossa of Rosenmüller, located superior and posterior to the torus tubarius
Because of the configuration of the torus tubarius, the fossa of Rosenmüller appears posterior on axial images and superior on coronal images to the eustachian tube orifice [2].
The adenoids, or pharyngeal tonsils, consist of lymphatic tissue located midline in the roof of the nasopharynx. Prominent adenoids are typically present in children. Gradual adenoidal involution begins around the time of puberty; the majority of the individuals have lost most of this adenoidal tissue by 30 years of age.
The pharyngobasilar fascia (Fig. 2b), a tough aponeurosis, separates the nasopharynx from the masticator space [3]. This pharyngobasilar fascia attaches to the skull base, anteriorly to the medial plate of the pterygoid process, and superiorly to the inferior part of the petrous apex. The foramen ovale is lateral to this fascia, while the foramen lacerum is within the attachment of this fascia to the skull base (Fig. 2). Posteriorly, the pharyngobasilar fascia attaches to the occipital pharyngeal tuber and the prevertebral muscles. The eustachian tube and levator veli palatini muscle enter the nasopharynx through a posterolateral defect of the pharyngobasilar fascia; this defect is known as the sinus of Morgagni.
The strong pharyngobasilar fascia limits tumor spread, but there are two points of weakness, representing privileged pathways for tumor spread:
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skull base and intracranial spread may occur through the foramen lacerum, despite the closure of this orifice by a fibro-cartilage
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posterolateral spread may occur through the sinus of Morgagni.
The pharyngobasilar fascia separates the nasopharynx from the deep facial spaces laterally: the prestyloid compartiment of the parapharyngeal space, and the retrostyloid compartiment of this space (essentially corresponding to the carotid space). The retropharyngeal space is located posteriorly, anterior to the prevertebral space. The retropharyngeal space is more or less continuous with the retrostyloid parapharyngeal space. Within the retropharyngeal space are the retropharyngeal nodes, constituting the primary nodal drainage of the nasopharynx.
Nasopharyngeal carcinomas
Histology
Most nasopharyngeal neoplasms are malignant tumors. Undifferentiated carcinoma is the most common form of malignancy, accounting for up to 98% of all nasopharyngeal malignancies in the Orient. The highest incidence rates are found in southern China and Hong Kong. Also, the southern rim of the Mediterranean is mostly affected. This represents the outcome of interactions of genetic factors, environmental factors and Epstein-Barr virus (EBV) infections. Patients with undifferentiated carcinoma show high levels of antibodies to EBV antigens [2, 5].
A variety of other malignancies arise in the nasopharynx, such as adenocarcinoma, cystic adenoid carcinoma, rhabdomyosarcomas and lymphoma.
Among benign nasopharyngeal lesions, prominent adenoids in children and teenagers are most common. Another benign lesion is a Thornwald cyst, a notochord derivative, which is a well-delineated cystic lesion, located midline in the roof of the nasopharynx.
Clinical presentation
Clinical complaints linked to nasopharyngeal tumors are usually subtle at the beginning. The average delay between the first symptoms and the discovery of the malignancy is 8–10 months.
The most common complaint at clinical presentation is cervical lymphadenopathy. In nasopharyngeal carcinoma, there is no relationship between the primary tumor size and the presence of nodal disease.
Other common presenting symptoms are otalgia, the sensation of an obstructed ear, or conductive hearing loss due to serous otitis, caused by eustachian tube obstruction. Imaging of the nasopharynx must be performed in the case of unilateral serous otitis in an adult, even if the clinical examination of the nasopharynx is normal.
Other symptoms include headaches, nasal obstruction and epistaxis.
Advanced tumors may present with neurologic symptoms such as headaches or palsies of cranial nerves.
Natural history
The fossa of Rosenmüller is a common site of origin of nasopharyngeal tumors (Fig. 3). Tumor tends to spread submucosally with early infiltration of the palatal muscles, in particular the levator veli palatini muscle. This muscle is responsible for opening of the eustachian tube orifice during swallowing, and its dysfunction results in serous otitis (Fig. 4).
The tumor will spread through areas of lesser resistance of the pharyngobasilar fascia, and into the deep spaces of the face.
Lymphadenopathy is present in up to 90% of the patients, the first involved site being the retropharyngeal nodal chain.
TNM classification
TNM classification was adapted in 2002, with the sixth edition of the nasopharyngeal carcinoma UICC TNM classification [6, 7] (Table 1). Some investigators have shown that tumor volume is an important prognostic factor [8, 9], and in the future, tumor volume may be incorporated into the nasopharyngeal carcinoma TNM classification.
Extension patterns on imaging
Imaging issues
The primary role of imaging is accurate tumor mapping with description of possible tumor extension to the skull base and the deep facial spaces. Magnetic resonance imaging (MRI) is more sensitive than computed tomography (CT) to detect perineural tumor spread and bone marrow changes in the skull base [3, 4]. However, early skull base erosion is best depicted on CT (Fig. 5).
Therefore, it may be useful to perform both a high resolution (HR) CT study of the skull base, and a MRI of the skull base and the neck.
The MRI study should be performed by using a dedicated head and neck coil, including the following sequences:
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HR turbo spin echo (TSE) T2-weighted sequence in the axial and coronal planes.
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HR spin echo (SE) T1-weighted sequence, without contrast or fat saturation in order to visualize skull base involvement showing modifications of the normal high signal in the bone marrow.
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Contrast-enhanced axial and coronal HR SE T1-weighted sequence with fat saturation.
This sequence is helpful to analyze deep extension, in particular perineural spread to the skull base and the endocranium. This sequence is also very useful to depict lateral spread to the prestyloid and retrostyloid compartiments of the parapharyngeal spaces, as well as the infratemporal fossa.
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TSE T2-weighted sequence in axial plane for the research of cervical lymph nodes including the supraclavicular fossa
Nasopharyngeal tumors, and especially undifferentiated carcinomas, usually present with intermediate signal intensity, superior to the muscle signal, on T2-weighted images, low signal intensity on T1-weighted images, and moderate enhancement (Fig. 3) on contrast-enhanced T1-weighted images, best defined with fat saturation [1, 10].
Tumoral spread
As explained, nasopharyngeal tumors spread along well-defined routes.
Anterior spread
Nasopharyngeal tumors often spread to the nasal fossa, which is not separated from the nasopharynx by any anatomic barrier. From the nasal fossa, the tumor may easily infiltrate the pterygopalatine fossa through the sphenopalatine foramen (Fig. 4). The earliest sign of involvement of the pterygopalatine fossa is replacement of its normal fat content by tumoral tissue (Fig. 6).
Once tumor gains access to the pterygopalatine fossa, it can spread into (Fig. 7):
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the foramen rotundum along the maxillary nerve (V2)
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the inferior orbital fissure and further the orbital apex, from where the tumor can extend intracranially through the superior orbital fissure.
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the infratemporal fossa, where the masticatory muscles are at risk of invasion. Erosion of the pterygoid process may occur. Perineural extension along the mandibular nerve (V3) into the foramen ovale and the endocranium is also possible (Fig. 7e)
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the vidian canal along the pterygoidien nerve and further to the petrous apex.
Lateral spread
Lateral extension to the parapharyngeal spaces can occur directly through the pharyngobasilar fascia (Fig. 8), or indirectly through the sinus of Morgagni, the fascia’s point of weakness. Further lateral spread involves the infratemporal fossa and the masticator space infiltrating the pterygoid muscles. From the masticator space, perineural extension along the mandibular nerve (V3) may occur, leading to infiltration of the foramen ovale and the cavernous sinus (Fig. 7e).
Posterior spread
Nasopharyngeal tumors can extend posteriorly to the retropharyngeal space and the prevertebral muscles (Fig. 9). Destruction of vertebral bodies is occasionally seen in very advanced tumors. Posterolateral extension may involve the jugular foramen and the hypoglossal canal (Fig. 10b), with possible but rare spread to the posterior fossa. This posterior extension may result in hypoglossal nerve (XII) palsy.
Inferior spread
Some nasopharyngeal tumors present with submucosal spread into the oropharynx, involving the tonsillar fossa (Fig. 11c). This extension may take place submucosally and thus escape detection by endoscopy, although not detection by imaging.
Superior spread
Nasopharyngeal tumor can spread through the foramen lacerum, even if it is contained by the pharyngobasilar fascia. If the tumor extends to the tough fibrous cartilage which closes the foramen lacerum, intracranial extension may occur (Fig. 12).
Superior spread with erosion of the clivus and the sphenoid sinus is also possible leading to intracranial extension (Fig. 5).
Intracranial extension of nasopharyngeal tumors is possible via different pathways such as the foramen lacerum, the foramen ovale and erosion of the skull base. Many studies have illustrated the good sensitivity of MRI to detect such extension, which is usually perineural. The frequency of intracranial abnormalities on MRI is 30% [2]. Nasopharyngeal tumors with intracranial extension are classified as T4 tumors according to the TNM staging system [2, 11]. Intracranial spread is usually extra-cerebral, resulting in involvement of the cavernous and temporal meninges.
Nodal metastasis
Cervical node metastasis is very common in nasopharyngeal tumors. It represents a usual initial presenting complaint.
The first nodes to be involved are the retropharyngeal nodes, and this is seen in 65% of nasopharyngeal tumors [2]. Lymphadenopathy at this location should be sought on imaging with attention (Fig. 11). It is interesting to note that involvement of retropharyngeal nodes does not appear in the TNM staging system as there is not sufficient evidence that these nodes affect the prognosis of the patient [12, 13].
In 75% of patients, enlarged cervical nodes are present, particularly high jugular nodes, sometimes without involvement of retropharyngeal nodes. For the N staging, the greatest dimension of the lymphadenopathy should be noticed, in particular in case of lymphadenothy greater than 6 cm (N3, stage IVB). Bilateral cervical lymphadenopathy may be seen in many patients. Supraclavicular fossa should be included in the analysis; in case of metastasis to lymph nodes in this location, the staging is IVB (Table 1) and the risk of distant metastasis is higher.
Distant metastasis
Nasopharyngeal tumors show a high frequency of distant metastases compared with other head and neck tumors, varying between 5% and 41% [2]. Patients with low cervical lymphadenopathy, especially in the supraclavicular fossa, and patients with important extension to the deep facial spaces, in particular the parapharyngeal space, have a significantly higher risk of distant metastases. The most common sites of metastases include bone (20%), lung (13%) and liver (9%) [14].
Diagnostic strategies
Two groups of patients require imaging:
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Patients presenting with clinical suspicion of nasopharyngeal tumor (serous otitis associated with cervical lymphadenopathy). Many studies have shown that MRI is superior to CT in demonstrating perineural extension and skull base marrow changes. It is also recommended to perform a CT scan on the skull base as discussed previously. Cervical node metastasis can either be evaluated on CT or MRI.
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Patients presenting with cervical lymphadenopathy without any known primary head and neck tumor. In this case, the entire aerodigestive tract should be analyzed carefully, including the nasopharynx, oropharynx, hypopharynx and larynx. Most teams prefer to obtain a contrast-enhanced CT scan from the skull base to the cervico-mediastinal orifice. If a nasopharyngeal tumor is suspected, a MRI should be performed in order to better demonstrate possible skull base extension.
A contrast-enhanced thoraco-abdominal CT scan, or PET-study, should be performed for T2b and/or N3 tumor to look for distant metastases. Most teams do this exam systematically [5].
Conclusion
Imaging is of particular interest in coming to a correct staging of the lesion. Extension of nasopharyngeal tumors, especially at the skull base and the deep facial spaces, is well illustrated on imaging. MRI best depicts perineural spread and bone marrow changes in the skull base, whereas CT is useful to detect early skull base erosion. Cervical node metastasis being very common in nasopharyngeal carcinomas, lymphadenopathy must be sought on imaging with attention.
A correct initial staging of the nasopharyngeal carcinoma is very important to perform the best treatment: small lesions (stage I and IIa) can be treated by radiotherapy alone, while larger lesions need heavier concomitant chemo-radiotherapy. The precise determination of the tumor borders is of great importance to determine the radiation portals.
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Dubrulle, F., Souillard, R. & Hermans, R. Extension patterns of nasopharyngeal carcinoma. Eur Radiol 17, 2622–2630 (2007). https://doi.org/10.1007/s00330-007-0616-z
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DOI: https://doi.org/10.1007/s00330-007-0616-z