PEER-REVIEW REPORTS
Gerardo Guinto1,2, Miguel Kageyama3, Vı´ctor H. Trujillo-Luarca1, Miguel Abdo1, Alberto Ruiz-Than1, Alberto Romero-Rangel1
Key words Approach - Infratemporal fossa - Jugular foramen - Nonglomic tumors - Skull base surgery -
Abbreviations and Acronyms CN: Cranial nerve CT: Computed tomography JF: Jugular foramen KPS: Karnofsky Performance Scale MRI: Magnetic resonance imaging From the 1Department of Neurosurgery, Hospital de Especialidades del Centro Medico Nacional Siglo XXI, Mexico City, Mexico; 2Centro Neurologico ABC, Mexico City, Mexico; and 3Department of Otolaryngology, Hospital de Especialidades del Centro Medico Nacional Siglo XXI, Mexico City, Mexico To whom correspondence should be addressed: Gerardo Guinto, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6:1283-1290. http://dx.doi.org/10.1016/j.wneu.2014.07.013 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
- OBJECTIVE:
Tumors of the jugular foramen are notably rare, and the majority of them arise from the glomic tissue of the jugular vein. There are other tumors that do not originate from that tissue, and these are called the nonglomic tumors. This report includes a series of patients with nonglomic tumors of the jugular foramen to analyze their biological and radiological behavior and the clinical outcomes of patients.
- METHODS:
Patients with tumors of the jugular foramen other than chemodectomas were included for the present series. All of the patients were subjected to a protocol that included imaging studies and a complete clinical evaluation. Surgery was planned and performed by a multidisciplinary team using the following approaches: retrosigmoid, infratemporal fossa, and zygomatic-transmandibular. Depending on the precise diagnosis and surgical outcomes, radiotherapy or radiosurgery were indicated. The average follow-up period was 5 years.
- RESULTS:
Thirty patients with nonglomic tumors were included: 18 schwannomas, 6 meningiomas, 5 chordomas, and 1 metastatic carcinoma. The patients with chordomas had the most severe clinical manifestations, and the chordomas were the largest and most invasive tumors that destroyed the jugular foramen contour on imaging studies. Schwannomas presented a more benign clinical evolution and enlarged (but did not destroy) the jugular foramen contour. Two patients died (chordomas) during the follow-up because of tumor activity.
- CONCLUSIONS:
INTRODUCTION
The most common nonglomic tumor of the jugular foramen was the schwannoma, which was the lesion with the best surgical prognosis. Chordoma is a rare and highly destructive tumor that has a notably high recurrence index.
The jugular foramen (JF) is a complex and deep structure located on the floor of the posterior fossa. The JF is divided by a fibrous, sometimes bony, septum into 2 segments: the pars nervosa and the pars vascularis. The pars nervosa is anteromedial, and the glossopharyngeal nerve (IX), the tympanic branch of the IX (Jacobson nerve), and the inferior petrosal sinus cross through this part. The pars vascularis is posterolateral, and the internal jugular vein, the vagus nerve (X), the accessory nerve (XI), and the auricular branch of the X (Arnold nerve) cross through it. Tumors that affect this region are rare. The majority of these tumors (60%e80% of the primary tumors) originate in the glomic tissue of the jugular vein (3, 6, 12, 14, 15). These tumors are known as chemodectomas, paragangliomas, or glomic tumors. The
most common nonglomic lesions in this region are schwannomas, which are followed by meningiomas and bony tumors (2, 24). Less frequently, metastases, carcinomas, or sarcomas are found. The signs and symptoms caused by tumors of the JF are similar among different tumor types (glomic and nonglomic) and in some cases, these tumors could be clinically confused with a cerebellopontine angle lesion. The clinical course is dominated by hearing loss, tinnitus, and/or alterations in the lower cranial nerves (CNs). Imaging studies are frequently nonspecific, and the precise diagnosis is commonly established after surgery. The management of these lesions is complex and requires a multidisciplinary
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY 82 [6]: 1283-1290, DECEMBER 2014
team that includes neurosurgery, otolaryngology, head and neck surgery, neurophysiology, and neuroradiology, among others. Because of the location and the size of these tumors, it is often necessary to carry out a combination of skull base approaches for their removal, which represents a nonnegligible risk for postoperative morbidity. Surgery of the JF is similar for glomic and nonglomic tumors, but paraganglioma cases typically are more challenging. Because of their high vascularity, glomic tumors require more complex preoperative procedures, such as angiography and selective embolization, and also require a wider exposure during their resection. This work helps neurosurgeons to identify nonglomic tumors and to
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Nonglomic Tumors of the Jugular Foramen: Differential Diagnosis and Prognostic Implications
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differentiate these tumors from chemodectomas before treatment, allowing for better diagnostic and surgical planning and avoiding unnecessary surgical risks. In the international literature, we did not identify another series that includes the wide variety of diagnoses presented in this report. PATIENTS AND METHODS We carried out a cross-sectional, retrospective, retrolective study of a case series from 1998 to 2008. All the patients with lesions of the JF other than chemodectomas who underwent operation in the Center of Skull Base Surgery of the Neurosurgery Service of the Hospital de Especialidades del Centro Medico Nacional Siglo XXI in Mexico City were analyzed. All the patients were included in a protocol in which they underwent comprehensive clinical evaluation, computed tomography (CT), and magnetic resonance imaging (MRI). The patients were subjected to surgery, and we planned the approach taking into account the specific tumor growth pattern. The portion of the tumor located on the posterior fossa was removed via a retrosigmoid approach, and the tumor component within the JF was removed via an infratemporal fossa approach (Fisch type “A”; Figure 1). For tumors presenting marked invasion of the infratemporal fossa, combinations of any of the previous approaches with zygomatic-transmandibular access were used (8) (Figure 2). Depending on the complexity of the approach, the surgeries were planned in 1, 2, or 3 surgical stages. Total removal was considered when no residual tumor was observed macroscopically in the surgical bed and in control imaging studies carried out 6 weeks after the intervention. Any evidence of new tumor activity subsequent to that time was named as a recurrence. Subtotal resection was considered if residual tumor was left only on the JF. All the remaining resections were considered as partial. Depending on the histopathologic diagnosis and surgical outcome, the patients were submitted to adjuvant treatment, which was predominantly radiotherapy or radiosurgery. The average follow-up period was 5 years (range, 2e12 years). Clinical assessments and imaging studies were carried out at least twice per year. The main goal of this series was to analyze the biological, clinical, and radiologic
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Figure 1. Infratemporal fossa approach. Left: Skin incision. Right: Tumor exposure. Note how anterior transposition of the facial nerve facilitates tumor excision. Carotid arteries, jugular vein, and lower cranial nerves are referred in the neck to assure vascular supply and nerve preservation.
behavior of nonglomic tumors to propose guidelines to establish a more accurate differential diagnosis before surgery. Clinical outcomes were evaluated to establish some prognostic implications in these cases. Statistical Analysis A descriptive analysis was performed regarding the signs, symptoms, imaging findings, surgical procedures, and evaluations of postoperative neurologic deficits.
An inferential analysis was conducted regarding the diagnostic imaging findings using quantitative variables (tumor volumes and dimensions) and semiquantitative nominal categories. For enhancement on CT and MRI, the following ranking system was applied: 0 ¼ null, 1 ¼ mild, 2 ¼ moderate, 3 ¼ intense, and 4 ¼ heterogeneous. The postoperative neurological status was evaluated in accordance with the deficit of at least 1 CN of the following 3 complexes:
Figure 2. Zygomatic-transmandibular approach. Left: Skin incision. Right: Bone management. Access to infratemporal fossa is obtained through a pterional craniotomy and an orbito-zygomatic and mandibular osteotomy. Ascending ramus of the mandible is cut and rotated upward (arrow) using the temporomandibular joint as a hinge. This approach was used only in huge tumors with ample invasion to infratemporal fossa.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.013
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Complex A: CN VII and VIII; Complex B: CN IX, X and XI; and Complex C: CN XII. The grading system was ranked as follows: Grade 0 ¼ no deficit; Grade 1 ¼ involvement of one complex; Grade 2 ¼ involvement of two complexes; Grade 3 ¼ involvement of three complexes; Grade 4 ¼ involvement of three complexes and unilateral motor deficit; Grade 5 ¼ involvement of three complexes and bilateral motor deficit; and Grade 6 ¼ death. A covariance analysis was applied to these variables. RESULTS During the 10-year study, there were 70 surgical patients with lesions in the JF. There were 40 chemodectomas and 30 nonglomic tumors included in this series. The average age was 41 years (range, 19e65 years); 19 patients were females, and 11 patients were males with the mode in the fifth and sixth decades of life. The histopathologic diagnoses were as follows: 18 schwannomas (60%), 6 meningiomas (20%), 5 chordomas (classical variety) (16.7%), and 1 metastatic carcinoma (3.3%). The average evolution time of clinical manifestations was 18 months (range, 9e36 months, mode 16 and 22 months). The predominant symptoms were dizziness (25 patients, 83%), headache (22, 73%), dysphagia (15, 50%), hearing loss (14, 46.67%), lateropulsion (12, 40%), and dysphonia (11, 36.6%). The most frequent clinical signs were involvement of CN VIII (20, 67%; 14 hearing deficit and 6 anacusia), CN X (17, 56%), lateropulsion (16, 53%), CN IX (11, 36.67%), and CN XI (11, 36.67%). Six patients (20%) showed alterations in the function of the facial nerve: 4 had paresis (13.33%), and 2 had paralysis (6.66%). Collet-Sicard was the most frequently observed JF syndrome (10, 33.33%). Because of the severity of the clinical manifestations, many patients experienced a significant effect on their quality of life; the average (M) score according to the Karnofsky Performance Scale (KPS) was 72.7 points. The patients with chordomas presented with the most significant effects on the quality of life (KPS M ¼ 61.3), and the least affected patients had schwannomas (KPS M ¼ 81.2). In the imaging studies, the schwannomas appeared as homogeneous (12, 55.56%), isodense lesions (13, 72.22%) with moderate contrast enhancement (13,
NONGLOMIC TUMORS OF THE JUGULAR FORAMEN
72.22%) on CT. On MRI T1-weighted phase imaging, schwannomas appeared as isointense (12, 66.67%), homogeneous lesions (15, 83.33%) with moderate enhancement with gadolinium. With respect to the JF, the most important characteristic of schwannomas was that they caused an evident increase in the dimensions of the foramen, but the tumors did not destroy the contour of the JF (Figure 3). The meningiomas were isodense (5, 83.33%), homogeneous lesions (6, 100%) with intense enhancement (4, 66.67%) on CT. On MRI T1-weighted imaging, the meningiomas appeared as isointense (6, 100%), homogeneous lesions (6, 100%) with moderate-tointense enhancement (3, 50%). There was no increase observed in the diameter of the JF with the meningiomas (Figure 4). The meningiomas could infiltrate 2 or more orifices of the skull base (Figure 5). The chordomas were the largest and most invasive lesions (Figure 6). The majority of chordomas were hypodense (4, 80%), homogeneous (4, 80%), and had mild contrast enhancement (4, 80%) on CT. On MRI, the chordomas were hypointense (4, 80%), homogeneous lesions (5, 100%) with mild gadolinium enhancement (3, 60%), and they eroded the foramen (3, 60%). There was a case of a giant chordoma with invasion of the cavernous sinus and infratemporal and pterygoid fossas (Figure 7). In normal CT coronal
sections with bone window algorithm performed in the region of the JF, the silhouette of an eagle’s head formed by the occipital condyle and the precondylar foramen is observed (16, 24). All of the chordomas altered this image (Figure 8). The most-often used approach in the present series was retrosigmoid (18 cases). In 10 patients with schwannomas and all the patients with meningiomas, the tumors were exclusively removed via this route. This approach was used in the case of a metastatic carcinoma. After an intraoperative diagnosis was made, only partial removal of the tumor was performed. In this particular case, the primary tumor was a papillary thyroid carcinoma, and the patient was subjected to radiotherapy with excellent results. The infratemporal approach was the next approach used most frequently in the present series. This approach was used in 13 cases: 8 patients with schwannoma who had a significant invasion of the JF and 5 patients with chordomas. In 7 of these 13 cases, it was necessary to perform an anterior transposition of the facial nerve. The zygomatictransmandibular approach was used in 2 cases (chordomas) in combination with infratemporal approach. In 13 (72.22%) patients with schwannomas, it was possible to achieve total tumor resection (Figure 9). In the other 5 patients, residual tumor was left in the JF (subtotal resection). All these patients were submitted to radiosurgery. In the 6 patients with
Figure 3. Axial T1-weighted magnetic resonance imaging with contrast enhancement of 2 typical schwannoma cases. Note how the tumor is enlarging but not destructing the JF. Left: Foraminal component of the tumor is very small. Right: The tumor inside the foramen is bigger.
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TUMOR Figure 4. Axial T1-weighted magnetic resonance imaging with contrast enhancement of a meningioma. The tumor is clearly invading the jugular foramen but without modifying its diameter.
meningiomas, the resection was subtotal (Figure 10). This residual tumor also was managed with radiosurgery in 4 cases. The other 2 patients did not accept this adjuvant therapy. The poorest surgical results were obtained with the chordomas. In the 5 cases, only partial resections could be performed (Figure 11). In the absence of the availability of heavy-charged-particle radiation, all the patients were subjected to standard external-beam radiotherapy. In this series, it was possible to improve the quality of life in almost all the patients, achieving an average of 87.8 points on the postoperative KPS. According to the grading system used in this series, the best
NONGLOMIC TUMORS OF THE JUGULAR FORAMEN
postoperative neurological status was observed in schwannomas, and the worst postoperative neurological status was observed in the chordomas (Table 1). The main morbidity was facial paresis, which arose especially in cases operated through the infratemporal approach where the anterior transposition of the facial nerve was required. In all but 2 cases, recovery was complete. In the present series, mortality was reported in 2 patients. One of these patients had a giant chordoma and had exacerbation of symptoms for 4 months postoperatively but rejected a new intervention. The patient’s condition progressively deteriorated until his death. The second patient also had a diagnosis of chordoma and died at 6 years of follow-up after 4 surgical reinterventions. The remainder of the patients with chordomas presented clinical and radiological signs of tumor regrowth during the follow-up period, but new surgeries have not been accepted by the patients. The patients in whom it was possible to achieve a total or subtotal resection plus radiosurgery did not show evidence of new tumor activity during the follow-up period. According to the covariance analysis carried out to determine the most important characteristics that help differentiate the preoperative diagnosis in these lesions, chordomas were distinguished by their larger maximum diameter (8.2 2.39 cm), mild enhancement on CT and MRI, and the destruction of the JF contours. Chordomas presented the poorest neurologic outcomes during follow-up (P < 0.05; Table 2).
Figure 5. Coronal T1-weighted magnetic resonance imaging with contrast enhancement of a meningioma. Tumor is invading several foramina of the skull base. Left: A small portion of the tumor is entering into the internal acoustic canal. Right: Tumor is growing towards the JF and foramen magnum.
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Figure 6. Sagittal T1-weighted magnetic resonance imaging of a chordoma. This tumor is big and highly destructive.
DISCUSSION The JF is a complex structure located in the floor of the posterior fossa, and it is described as a channel that courses in an oblique, anterior, inferior, and lateral direction. It is found posterolaterally to the carotid channel, between the petrous portion of the temporal bone and the occipital squama (2, 15, 17). Glomic tumors are the lesions found with the greatest frequency in this region (3, 6, 12, 14, 15), and only 20%e40% of lesions are other types of tumors. In our series, the frequency of nonglomic tumors was 42.85%, which is similar to the frequency published in the international literature. Nonglomic tumors of the JF could be classified as intrinsic (arising from structures normally found in the foramen) or extrinsic (arising from adjacent structures). The most common intrinsic tumors are lower CN schwannomas (2, 24); our findings were consistent with this. The list of extrinsic tumors is very large and includes vestibular
Figure 7. Coronal T1-weighted magnetic resonance imaging with contrast enhancement of a giant chorodma.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.013
PEER-REVIEW REPORTS NONGLOMIC TUMORS OF THE JUGULAR FORAMEN
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GERARDO GUINTO ET AL.
Figure 8. Coronal computed tomography with bone window algorithm in the JF. Note how on the right side, the normal occipital condyle and the precondylar foramen show an eagle’s head shape (black arrow). On the left side, the tumor (chordoma) is altering this image (white arrow). JF, jugular foramen.
schwannomas, meningiomas, chordomas and chondrosarcomas, chondroblastomas, osteoclastomas, fibrosarcomas, tumors of the endolymphatic sac, malignant tumors of the temporal bone, cholesteatomas, epidermoid tumors, primitive neuroectodermic tumors, and lung, breast, and prostate metastases (6, 14, 21, 22). In our series, one of the most frequent secondary tumors was the clivus chordoma, which does not coincide with what has been reported in similar series. The high frequency of chordomas presented in this study demonstrates that these tumors are not always located in the midline. Their lateral location is explained by remnants of the notochord that might be found disseminated throughout the entire skull base (9). We confirmed that the main clinical manifestations of nonglomic tumors of the JF are dizziness, headache, and hearing problems. For this reason, these lesions could be confused with tumors located on the cerebellopontine angle. If we consider the relatively high index of CN X involvement (56%) and CN IX and XI involvement (36% each), these clinical manifestations might help to make preoperative differential diagnoses. The clinical presentation of paragangliomas is similar, but these tumors present a greater index of tinnitus (constant or pulsatile). Schwannomas of the JF occur in 0.17%e 0.72% of intracranial tumors (2, 10, 20, 22, 25, 26) and represent 10%e30% of the tumors in this region (26), which is in agreement with the 25.71% found in the
Figure 9. Surgical results in schwannomas. In the majority of cases, the tumors were entirely removed. Preoperative images are on the left and postoperative on the right.
present series. These are benign, slowgrowing lesions whose origin is, in order of frequency, CNs X, IX, and XI, which we found in our patients. For large tumors especially, it is not always possible to precisely define the exact nerve of origin for the tumor (4, 18, 21, 23). These tumors might originate from the cisternal, foraminal, or extracranial portion of the lower CNs. When the tumors arise in the cisternal portion, they present greater intracranial growth and are relatively easy to remove via a simple retrosigmoid approach. The tumors that originate from the foraminal portion tend to have a mixed growth towards the cistern and towards the foramen, and their removal depends on the location of the greatest portion of the tumor. In cases in which the foraminal component is very extensive, a retrosigmoid approach is insufficient because the bottom of the JF
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remains hidden from the surgeon’s view. It is not possible to gain access to this foramen via the retrosigmoid approach by bone drilling (as is performed in cases of vestibular schwannomas) because of the presence of the sigmoid sinus. For this reason, a wider exposure of the foramen becomes necessary in these cases, and an infratemporal approach represents an excellent option. With the recent advances in endoscopy, this has become an extremely useful tool for removing the tumor component within the foramen via a retrosigmoid approach. There are rare cases in which schwannomas originate in the extracranial portion of the JF, showing a growth predominantly towards the infratemporal fossa. In these cases, the tumors usually are located medial to the ascending root of the mandible, which will need to be
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Table 1. Postoperative Neurologic Status Grade
TUMOR
Tumor
0
1
2
3
Schwannoma
6
4
2
6
Meningioma
2
Chordoma
2
1
1
2
Carcinoma Total
Figure 10. Surgical results in meningiomas. In all cases the posterior fossa component of the tumor could be completely removed, but leaving a small piece of it inside the JF. Preoperative images are on the left and postoperative on the right. JF, jugular foramen.
Figure 11. Surgical results in chordomas. Only a partial resection could be achieved. Preoperative image is on the left and postoperative on the right.
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4
5
6
1
1
1
1
1
1 8
7
3
9
1
mobilized during the surgical approach to achieve better exposure (8, 10, 11). In our series, all the schwannomas had a mixed presentation, i.e., both cisternal and foraminal, but had greater growth towards the cistern. For this reason, successful removal was achieved in the majority of cases exclusively through a retrosigmoid approach. If the foraminal portion of the tumor could not be removed with surgery or endoscopy in similar cases, radiosurgery is an excellent option for obtaining good long-term control of the disease. The radiologic diagnosis of schwannomas of the JF is relatively simple because these tumors are well-defined lesions with moderate and homogeneous contrast enhancement, which expand (and not erode) the foramen; these findings were confirmed in the present series. We observed that these tumors represent a better prognosis because they are slow-growing lesions that could generally be removed with almost no morbidity. Meningiomas of the JF represent approximately 0.7%e4% of the meningiomas of the posterior fossa (1, 7, 13, 19). They are the third most frequently found tumor in this location, which is consistent with our findings. The CN affected with the greatest frequency by meningiomas is CN X (53.8%), followed by CN XI (23%) (19); these findings were confirmed in the present series. Those lesions might be considered as intrinsic and extrinsic in the foramen. Intrinsic lesions originate in the arachnoid villi adjacent to the jugular bulb and tend to be confined to the interior of the foramen, but they could invade the infralabyrinthine region and the middle ear or extend towards the cerebellopontine angle and/or towards higher regions of the neck (19, 24). Extrinsic meningiomas originate in the arachnoid
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.013
PEER-REVIEW REPORTS NONGLOMIC TUMORS OF THE JUGULAR FORAMEN
Table 2. Statistically Significant Findings in Chordomas Compared with Meningiomas and Schwannomas PosHoc (P
Gerardo Guinto1,2, Miguel Kageyama3, Vı´ctor H. Trujillo-Luarca1, Miguel Abdo1, Alberto Ruiz-Than1, Alberto Romero-Rangel1
Key words Approach - Infratemporal fossa - Jugular foramen - Nonglomic tumors - Skull base surgery -
Abbreviations and Acronyms CN: Cranial nerve CT: Computed tomography JF: Jugular foramen KPS: Karnofsky Performance Scale MRI: Magnetic resonance imaging From the 1Department of Neurosurgery, Hospital de Especialidades del Centro Medico Nacional Siglo XXI, Mexico City, Mexico; 2Centro Neurologico ABC, Mexico City, Mexico; and 3Department of Otolaryngology, Hospital de Especialidades del Centro Medico Nacional Siglo XXI, Mexico City, Mexico To whom correspondence should be addressed: Gerardo Guinto, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6:1283-1290. http://dx.doi.org/10.1016/j.wneu.2014.07.013 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
- OBJECTIVE:
Tumors of the jugular foramen are notably rare, and the majority of them arise from the glomic tissue of the jugular vein. There are other tumors that do not originate from that tissue, and these are called the nonglomic tumors. This report includes a series of patients with nonglomic tumors of the jugular foramen to analyze their biological and radiological behavior and the clinical outcomes of patients.
- METHODS:
Patients with tumors of the jugular foramen other than chemodectomas were included for the present series. All of the patients were subjected to a protocol that included imaging studies and a complete clinical evaluation. Surgery was planned and performed by a multidisciplinary team using the following approaches: retrosigmoid, infratemporal fossa, and zygomatic-transmandibular. Depending on the precise diagnosis and surgical outcomes, radiotherapy or radiosurgery were indicated. The average follow-up period was 5 years.
- RESULTS:
Thirty patients with nonglomic tumors were included: 18 schwannomas, 6 meningiomas, 5 chordomas, and 1 metastatic carcinoma. The patients with chordomas had the most severe clinical manifestations, and the chordomas were the largest and most invasive tumors that destroyed the jugular foramen contour on imaging studies. Schwannomas presented a more benign clinical evolution and enlarged (but did not destroy) the jugular foramen contour. Two patients died (chordomas) during the follow-up because of tumor activity.
- CONCLUSIONS:
INTRODUCTION
The most common nonglomic tumor of the jugular foramen was the schwannoma, which was the lesion with the best surgical prognosis. Chordoma is a rare and highly destructive tumor that has a notably high recurrence index.
The jugular foramen (JF) is a complex and deep structure located on the floor of the posterior fossa. The JF is divided by a fibrous, sometimes bony, septum into 2 segments: the pars nervosa and the pars vascularis. The pars nervosa is anteromedial, and the glossopharyngeal nerve (IX), the tympanic branch of the IX (Jacobson nerve), and the inferior petrosal sinus cross through this part. The pars vascularis is posterolateral, and the internal jugular vein, the vagus nerve (X), the accessory nerve (XI), and the auricular branch of the X (Arnold nerve) cross through it. Tumors that affect this region are rare. The majority of these tumors (60%e80% of the primary tumors) originate in the glomic tissue of the jugular vein (3, 6, 12, 14, 15). These tumors are known as chemodectomas, paragangliomas, or glomic tumors. The
most common nonglomic lesions in this region are schwannomas, which are followed by meningiomas and bony tumors (2, 24). Less frequently, metastases, carcinomas, or sarcomas are found. The signs and symptoms caused by tumors of the JF are similar among different tumor types (glomic and nonglomic) and in some cases, these tumors could be clinically confused with a cerebellopontine angle lesion. The clinical course is dominated by hearing loss, tinnitus, and/or alterations in the lower cranial nerves (CNs). Imaging studies are frequently nonspecific, and the precise diagnosis is commonly established after surgery. The management of these lesions is complex and requires a multidisciplinary
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY 82 [6]: 1283-1290, DECEMBER 2014
team that includes neurosurgery, otolaryngology, head and neck surgery, neurophysiology, and neuroradiology, among others. Because of the location and the size of these tumors, it is often necessary to carry out a combination of skull base approaches for their removal, which represents a nonnegligible risk for postoperative morbidity. Surgery of the JF is similar for glomic and nonglomic tumors, but paraganglioma cases typically are more challenging. Because of their high vascularity, glomic tumors require more complex preoperative procedures, such as angiography and selective embolization, and also require a wider exposure during their resection. This work helps neurosurgeons to identify nonglomic tumors and to
www.WORLDNEUROSURGERY.org
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TUMOR
Nonglomic Tumors of the Jugular Foramen: Differential Diagnosis and Prognostic Implications
PEER-REVIEW REPORTS GERARDO GUINTO ET AL.
NONGLOMIC TUMORS OF THE JUGULAR FORAMEN
TUMOR
differentiate these tumors from chemodectomas before treatment, allowing for better diagnostic and surgical planning and avoiding unnecessary surgical risks. In the international literature, we did not identify another series that includes the wide variety of diagnoses presented in this report. PATIENTS AND METHODS We carried out a cross-sectional, retrospective, retrolective study of a case series from 1998 to 2008. All the patients with lesions of the JF other than chemodectomas who underwent operation in the Center of Skull Base Surgery of the Neurosurgery Service of the Hospital de Especialidades del Centro Medico Nacional Siglo XXI in Mexico City were analyzed. All the patients were included in a protocol in which they underwent comprehensive clinical evaluation, computed tomography (CT), and magnetic resonance imaging (MRI). The patients were subjected to surgery, and we planned the approach taking into account the specific tumor growth pattern. The portion of the tumor located on the posterior fossa was removed via a retrosigmoid approach, and the tumor component within the JF was removed via an infratemporal fossa approach (Fisch type “A”; Figure 1). For tumors presenting marked invasion of the infratemporal fossa, combinations of any of the previous approaches with zygomatic-transmandibular access were used (8) (Figure 2). Depending on the complexity of the approach, the surgeries were planned in 1, 2, or 3 surgical stages. Total removal was considered when no residual tumor was observed macroscopically in the surgical bed and in control imaging studies carried out 6 weeks after the intervention. Any evidence of new tumor activity subsequent to that time was named as a recurrence. Subtotal resection was considered if residual tumor was left only on the JF. All the remaining resections were considered as partial. Depending on the histopathologic diagnosis and surgical outcome, the patients were submitted to adjuvant treatment, which was predominantly radiotherapy or radiosurgery. The average follow-up period was 5 years (range, 2e12 years). Clinical assessments and imaging studies were carried out at least twice per year. The main goal of this series was to analyze the biological, clinical, and radiologic
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Figure 1. Infratemporal fossa approach. Left: Skin incision. Right: Tumor exposure. Note how anterior transposition of the facial nerve facilitates tumor excision. Carotid arteries, jugular vein, and lower cranial nerves are referred in the neck to assure vascular supply and nerve preservation.
behavior of nonglomic tumors to propose guidelines to establish a more accurate differential diagnosis before surgery. Clinical outcomes were evaluated to establish some prognostic implications in these cases. Statistical Analysis A descriptive analysis was performed regarding the signs, symptoms, imaging findings, surgical procedures, and evaluations of postoperative neurologic deficits.
An inferential analysis was conducted regarding the diagnostic imaging findings using quantitative variables (tumor volumes and dimensions) and semiquantitative nominal categories. For enhancement on CT and MRI, the following ranking system was applied: 0 ¼ null, 1 ¼ mild, 2 ¼ moderate, 3 ¼ intense, and 4 ¼ heterogeneous. The postoperative neurological status was evaluated in accordance with the deficit of at least 1 CN of the following 3 complexes:
Figure 2. Zygomatic-transmandibular approach. Left: Skin incision. Right: Bone management. Access to infratemporal fossa is obtained through a pterional craniotomy and an orbito-zygomatic and mandibular osteotomy. Ascending ramus of the mandible is cut and rotated upward (arrow) using the temporomandibular joint as a hinge. This approach was used only in huge tumors with ample invasion to infratemporal fossa.
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Complex A: CN VII and VIII; Complex B: CN IX, X and XI; and Complex C: CN XII. The grading system was ranked as follows: Grade 0 ¼ no deficit; Grade 1 ¼ involvement of one complex; Grade 2 ¼ involvement of two complexes; Grade 3 ¼ involvement of three complexes; Grade 4 ¼ involvement of three complexes and unilateral motor deficit; Grade 5 ¼ involvement of three complexes and bilateral motor deficit; and Grade 6 ¼ death. A covariance analysis was applied to these variables. RESULTS During the 10-year study, there were 70 surgical patients with lesions in the JF. There were 40 chemodectomas and 30 nonglomic tumors included in this series. The average age was 41 years (range, 19e65 years); 19 patients were females, and 11 patients were males with the mode in the fifth and sixth decades of life. The histopathologic diagnoses were as follows: 18 schwannomas (60%), 6 meningiomas (20%), 5 chordomas (classical variety) (16.7%), and 1 metastatic carcinoma (3.3%). The average evolution time of clinical manifestations was 18 months (range, 9e36 months, mode 16 and 22 months). The predominant symptoms were dizziness (25 patients, 83%), headache (22, 73%), dysphagia (15, 50%), hearing loss (14, 46.67%), lateropulsion (12, 40%), and dysphonia (11, 36.6%). The most frequent clinical signs were involvement of CN VIII (20, 67%; 14 hearing deficit and 6 anacusia), CN X (17, 56%), lateropulsion (16, 53%), CN IX (11, 36.67%), and CN XI (11, 36.67%). Six patients (20%) showed alterations in the function of the facial nerve: 4 had paresis (13.33%), and 2 had paralysis (6.66%). Collet-Sicard was the most frequently observed JF syndrome (10, 33.33%). Because of the severity of the clinical manifestations, many patients experienced a significant effect on their quality of life; the average (M) score according to the Karnofsky Performance Scale (KPS) was 72.7 points. The patients with chordomas presented with the most significant effects on the quality of life (KPS M ¼ 61.3), and the least affected patients had schwannomas (KPS M ¼ 81.2). In the imaging studies, the schwannomas appeared as homogeneous (12, 55.56%), isodense lesions (13, 72.22%) with moderate contrast enhancement (13,
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72.22%) on CT. On MRI T1-weighted phase imaging, schwannomas appeared as isointense (12, 66.67%), homogeneous lesions (15, 83.33%) with moderate enhancement with gadolinium. With respect to the JF, the most important characteristic of schwannomas was that they caused an evident increase in the dimensions of the foramen, but the tumors did not destroy the contour of the JF (Figure 3). The meningiomas were isodense (5, 83.33%), homogeneous lesions (6, 100%) with intense enhancement (4, 66.67%) on CT. On MRI T1-weighted imaging, the meningiomas appeared as isointense (6, 100%), homogeneous lesions (6, 100%) with moderate-tointense enhancement (3, 50%). There was no increase observed in the diameter of the JF with the meningiomas (Figure 4). The meningiomas could infiltrate 2 or more orifices of the skull base (Figure 5). The chordomas were the largest and most invasive lesions (Figure 6). The majority of chordomas were hypodense (4, 80%), homogeneous (4, 80%), and had mild contrast enhancement (4, 80%) on CT. On MRI, the chordomas were hypointense (4, 80%), homogeneous lesions (5, 100%) with mild gadolinium enhancement (3, 60%), and they eroded the foramen (3, 60%). There was a case of a giant chordoma with invasion of the cavernous sinus and infratemporal and pterygoid fossas (Figure 7). In normal CT coronal
sections with bone window algorithm performed in the region of the JF, the silhouette of an eagle’s head formed by the occipital condyle and the precondylar foramen is observed (16, 24). All of the chordomas altered this image (Figure 8). The most-often used approach in the present series was retrosigmoid (18 cases). In 10 patients with schwannomas and all the patients with meningiomas, the tumors were exclusively removed via this route. This approach was used in the case of a metastatic carcinoma. After an intraoperative diagnosis was made, only partial removal of the tumor was performed. In this particular case, the primary tumor was a papillary thyroid carcinoma, and the patient was subjected to radiotherapy with excellent results. The infratemporal approach was the next approach used most frequently in the present series. This approach was used in 13 cases: 8 patients with schwannoma who had a significant invasion of the JF and 5 patients with chordomas. In 7 of these 13 cases, it was necessary to perform an anterior transposition of the facial nerve. The zygomatictransmandibular approach was used in 2 cases (chordomas) in combination with infratemporal approach. In 13 (72.22%) patients with schwannomas, it was possible to achieve total tumor resection (Figure 9). In the other 5 patients, residual tumor was left in the JF (subtotal resection). All these patients were submitted to radiosurgery. In the 6 patients with
Figure 3. Axial T1-weighted magnetic resonance imaging with contrast enhancement of 2 typical schwannoma cases. Note how the tumor is enlarging but not destructing the JF. Left: Foraminal component of the tumor is very small. Right: The tumor inside the foramen is bigger.
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TUMOR Figure 4. Axial T1-weighted magnetic resonance imaging with contrast enhancement of a meningioma. The tumor is clearly invading the jugular foramen but without modifying its diameter.
meningiomas, the resection was subtotal (Figure 10). This residual tumor also was managed with radiosurgery in 4 cases. The other 2 patients did not accept this adjuvant therapy. The poorest surgical results were obtained with the chordomas. In the 5 cases, only partial resections could be performed (Figure 11). In the absence of the availability of heavy-charged-particle radiation, all the patients were subjected to standard external-beam radiotherapy. In this series, it was possible to improve the quality of life in almost all the patients, achieving an average of 87.8 points on the postoperative KPS. According to the grading system used in this series, the best
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postoperative neurological status was observed in schwannomas, and the worst postoperative neurological status was observed in the chordomas (Table 1). The main morbidity was facial paresis, which arose especially in cases operated through the infratemporal approach where the anterior transposition of the facial nerve was required. In all but 2 cases, recovery was complete. In the present series, mortality was reported in 2 patients. One of these patients had a giant chordoma and had exacerbation of symptoms for 4 months postoperatively but rejected a new intervention. The patient’s condition progressively deteriorated until his death. The second patient also had a diagnosis of chordoma and died at 6 years of follow-up after 4 surgical reinterventions. The remainder of the patients with chordomas presented clinical and radiological signs of tumor regrowth during the follow-up period, but new surgeries have not been accepted by the patients. The patients in whom it was possible to achieve a total or subtotal resection plus radiosurgery did not show evidence of new tumor activity during the follow-up period. According to the covariance analysis carried out to determine the most important characteristics that help differentiate the preoperative diagnosis in these lesions, chordomas were distinguished by their larger maximum diameter (8.2 2.39 cm), mild enhancement on CT and MRI, and the destruction of the JF contours. Chordomas presented the poorest neurologic outcomes during follow-up (P < 0.05; Table 2).
Figure 5. Coronal T1-weighted magnetic resonance imaging with contrast enhancement of a meningioma. Tumor is invading several foramina of the skull base. Left: A small portion of the tumor is entering into the internal acoustic canal. Right: Tumor is growing towards the JF and foramen magnum.
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Figure 6. Sagittal T1-weighted magnetic resonance imaging of a chordoma. This tumor is big and highly destructive.
DISCUSSION The JF is a complex structure located in the floor of the posterior fossa, and it is described as a channel that courses in an oblique, anterior, inferior, and lateral direction. It is found posterolaterally to the carotid channel, between the petrous portion of the temporal bone and the occipital squama (2, 15, 17). Glomic tumors are the lesions found with the greatest frequency in this region (3, 6, 12, 14, 15), and only 20%e40% of lesions are other types of tumors. In our series, the frequency of nonglomic tumors was 42.85%, which is similar to the frequency published in the international literature. Nonglomic tumors of the JF could be classified as intrinsic (arising from structures normally found in the foramen) or extrinsic (arising from adjacent structures). The most common intrinsic tumors are lower CN schwannomas (2, 24); our findings were consistent with this. The list of extrinsic tumors is very large and includes vestibular
Figure 7. Coronal T1-weighted magnetic resonance imaging with contrast enhancement of a giant chorodma.
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Figure 8. Coronal computed tomography with bone window algorithm in the JF. Note how on the right side, the normal occipital condyle and the precondylar foramen show an eagle’s head shape (black arrow). On the left side, the tumor (chordoma) is altering this image (white arrow). JF, jugular foramen.
schwannomas, meningiomas, chordomas and chondrosarcomas, chondroblastomas, osteoclastomas, fibrosarcomas, tumors of the endolymphatic sac, malignant tumors of the temporal bone, cholesteatomas, epidermoid tumors, primitive neuroectodermic tumors, and lung, breast, and prostate metastases (6, 14, 21, 22). In our series, one of the most frequent secondary tumors was the clivus chordoma, which does not coincide with what has been reported in similar series. The high frequency of chordomas presented in this study demonstrates that these tumors are not always located in the midline. Their lateral location is explained by remnants of the notochord that might be found disseminated throughout the entire skull base (9). We confirmed that the main clinical manifestations of nonglomic tumors of the JF are dizziness, headache, and hearing problems. For this reason, these lesions could be confused with tumors located on the cerebellopontine angle. If we consider the relatively high index of CN X involvement (56%) and CN IX and XI involvement (36% each), these clinical manifestations might help to make preoperative differential diagnoses. The clinical presentation of paragangliomas is similar, but these tumors present a greater index of tinnitus (constant or pulsatile). Schwannomas of the JF occur in 0.17%e 0.72% of intracranial tumors (2, 10, 20, 22, 25, 26) and represent 10%e30% of the tumors in this region (26), which is in agreement with the 25.71% found in the
Figure 9. Surgical results in schwannomas. In the majority of cases, the tumors were entirely removed. Preoperative images are on the left and postoperative on the right.
present series. These are benign, slowgrowing lesions whose origin is, in order of frequency, CNs X, IX, and XI, which we found in our patients. For large tumors especially, it is not always possible to precisely define the exact nerve of origin for the tumor (4, 18, 21, 23). These tumors might originate from the cisternal, foraminal, or extracranial portion of the lower CNs. When the tumors arise in the cisternal portion, they present greater intracranial growth and are relatively easy to remove via a simple retrosigmoid approach. The tumors that originate from the foraminal portion tend to have a mixed growth towards the cistern and towards the foramen, and their removal depends on the location of the greatest portion of the tumor. In cases in which the foraminal component is very extensive, a retrosigmoid approach is insufficient because the bottom of the JF
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remains hidden from the surgeon’s view. It is not possible to gain access to this foramen via the retrosigmoid approach by bone drilling (as is performed in cases of vestibular schwannomas) because of the presence of the sigmoid sinus. For this reason, a wider exposure of the foramen becomes necessary in these cases, and an infratemporal approach represents an excellent option. With the recent advances in endoscopy, this has become an extremely useful tool for removing the tumor component within the foramen via a retrosigmoid approach. There are rare cases in which schwannomas originate in the extracranial portion of the JF, showing a growth predominantly towards the infratemporal fossa. In these cases, the tumors usually are located medial to the ascending root of the mandible, which will need to be
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Table 1. Postoperative Neurologic Status Grade
TUMOR
Tumor
0
1
2
3
Schwannoma
6
4
2
6
Meningioma
2
Chordoma
2
1
1
2
Carcinoma Total
Figure 10. Surgical results in meningiomas. In all cases the posterior fossa component of the tumor could be completely removed, but leaving a small piece of it inside the JF. Preoperative images are on the left and postoperative on the right. JF, jugular foramen.
Figure 11. Surgical results in chordomas. Only a partial resection could be achieved. Preoperative image is on the left and postoperative on the right.
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4
5
6
1
1
1
1
1
1 8
7
3
9
1
mobilized during the surgical approach to achieve better exposure (8, 10, 11). In our series, all the schwannomas had a mixed presentation, i.e., both cisternal and foraminal, but had greater growth towards the cistern. For this reason, successful removal was achieved in the majority of cases exclusively through a retrosigmoid approach. If the foraminal portion of the tumor could not be removed with surgery or endoscopy in similar cases, radiosurgery is an excellent option for obtaining good long-term control of the disease. The radiologic diagnosis of schwannomas of the JF is relatively simple because these tumors are well-defined lesions with moderate and homogeneous contrast enhancement, which expand (and not erode) the foramen; these findings were confirmed in the present series. We observed that these tumors represent a better prognosis because they are slow-growing lesions that could generally be removed with almost no morbidity. Meningiomas of the JF represent approximately 0.7%e4% of the meningiomas of the posterior fossa (1, 7, 13, 19). They are the third most frequently found tumor in this location, which is consistent with our findings. The CN affected with the greatest frequency by meningiomas is CN X (53.8%), followed by CN XI (23%) (19); these findings were confirmed in the present series. Those lesions might be considered as intrinsic and extrinsic in the foramen. Intrinsic lesions originate in the arachnoid villi adjacent to the jugular bulb and tend to be confined to the interior of the foramen, but they could invade the infralabyrinthine region and the middle ear or extend towards the cerebellopontine angle and/or towards higher regions of the neck (19, 24). Extrinsic meningiomas originate in the arachnoid
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Table 2. Statistically Significant Findings in Chordomas Compared with Meningiomas and Schwannomas PosHoc (P
