Perspectives Commentary on: Nonglomic Tumors of the Jugular Foramen: Differential Diagnosis and Prognostic Implications by Guinto et al. World Neurosurg 82:1283-1290, 2014
Diverse Pathologies of the Jugular Foramen Anil Nanda and Richard D. Murray
T
he posterior fossa presents a fascinatingly complex anatomical region that includes not only vital brainstem structures but also delicate cranial nerves in close proximity to major vascular structures. Once anatomical variation and tumor distortion are superimposed on this complex region, addressing lesions in this region presents unique challenges to skull base surgeons. Lesions of the jugular foramen are prime examples of these challenges. The sigmoid sinus and inferior petrosal sinus closely interact with the IXth, Xth, and XIth cranial nerves, all of which are located in a deep and medial corner of the posterior fossa, with the brainstem and rigid bony confines limiting access to this area. In a recent issue of WORLD NEUROSURGERY, Guinto et al. performed a comprehensive review of their 10-year experience in managing the unique pathology of this region. During this period, they operated on 70 patients with lesions involving the jugular foramen, 30 of which were nonglomic tumors. They then retrospectively studied these nonglomic tumors, which consisted of 18 schwannomas, 6 meningiomas, 5 chordomas, and 1 metastasis and documented their operative approach, surgical results, and preoperative imaging findings. All of their patients were actively symptomatic at time of presentation. As expected by the basic biology of the respective tumors, the patients with schwannoma and meningiomas tended to fare better in the long term, whereas patients with chordomas demonstrated a recurrent and relentless course, with 2 patients eventually succumbing to this disease. All of the authors’ patients were symptomatic at the time of presentation, and they elegantly highlight how preoperative imaging studies were useful in predicting the intraoperative pathology. Their surgical
Key words Approach - Infratemporal fossa - Jugular foramen - Nonglomic tumors - Skull base surgery -
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outcomes speak to their extensive experience with dealing with such divergent pathologies that all involve the jugular foramen. Since the early 1900s when a variety of eponymous jugular foramen syndromes (Vernet, Collet-Sicard, etc) (2, 15) were first described, it has been well known that these constellations of neurologic signs can be caused by a variety of pathologies, ranging from benign to malignant tumors, ischemic and inflammatory events to cranial nerves, fractures of the skull base, and penetrating as well as blunt trauma. Neoplastic pathologies encountered in this region are diverse, with the most common being glomus jugulare tumors, which arise from paraganglia within the jugular adventitia (56%e77%) (11, 13, 16). These tend to have a characteristic growth pattern, being unencapsulated and infiltrating along tissue planes and pathways of least resistance, invading air cells, vascular lumens, skull base foramina, and the Eustachian tube (8, 16). Other pathologies, although less common, are nevertheless encountered. Nerve sheath tumors arise from the glossopharyngeal (IX), vagus (X), and accessory (XI) nerves (16). Meningiomas can originate either in the posterior fossa and grow to involve the jugular foramen or more rarely can have their epicenter in the jugular foramen itself and spread into the posterior fossa (16). They may have either a centrifugal growth pattern, growing in all directions from their epicenter, or they may exhibit an en plaque pattern, spreading along dural reflections (9, 16). Chordomas, although typically arising in the clivus and sphenooccipital synchondrosis, can grow eccentrically and involve the petrous bone and the jugular foramen (7, 10, 16). Other pathologies in this region may include various metastatic tumors, hemangiopericytoma, plasmacytoma, etc (11).
Department of Neurosurgery, Louisiana State University Health Sciences Center in Shreveport, Shreveport, Louisiana, USA To whom correspondence should be addressed: Anil Nanda, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 83, 2:164-166. http://dx.doi.org/10.1016/j.wneu.2014.11.008
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.11.008
PERSPECTIVES
Given the delicacy of structures in this region, the importance of cranial nerve efferent control over primitive functions such as swallowing and the prevention of aspiration, the relative lack of redundancy in these structures, coupled with the spatial crowding of this area, it is not surprising that interventions in this region tend to be fraught with risk. Lower cranial nerve dysfunction after surgery has a major impact on patient quality of life (3, 6, 8, 13, 14). Even relatively minor disturbances in swallowing function, although not always readily elicited during routine postoperative office visits, can have a very significant detriment to nutritional intake and quality of life (3). Pheochromocytomas and paragangliomas have the greatest degree of heritability of all human tumors, at approximately 40%. Approximately 40% of these carry a germline mutation in 1 of at least 12 genes. Within the last decade, a genetic driver event has been elucidated in roughly 50% of these lesions. These lesion play a unique role in the study of human cancer genetic mechanisms and have played a substantial role in our understanding of cancer biology (4). Concomitantly with the clarification of the different pathologies in this area, medical advances are ever improving our ability to address these pathologies. Magnetic resonance imaging can demonstrate extent of tumor infiltration, growth patterns, and spread. Computed tomography provides detailed bony anatomy and evaluation of the jugular foramen to demonstrate bony enlargement without destruction, especially in cases of schwannomas. Angiography is helpful in differentiating paragangliomas from other pathologies but also can help to demonstrate tumor blush and origin of feeding vessels, which can then be followed by judicious embolization. Balloon test occlusion studies help to predict whether occlusion of the petrous internal carotid artery would be tolerated. Nerve monitoring techniques help to warn surgeons of impending lower cranial nerve damage. Judicious use of endoscopy has evolved to enable smaller incisions and tailored trajectories. Microsurgical techniques and familiarity with skull base approaches has previously considered inoperable tumors to be managed successfully (1). Perhaps the most profound advance has been the role of radiotherapy in the management of these lesions. Proton beam therapy has established a strong role in the postsurgical management of skull base chordomas. Stereotactic radiosurgery has an ever-advancing role, not just as salvage option for tumor residuals postsurgery but also as a primary treatment modality for well-selected tumors, demonstrating a cessation of tumor growth with minimal side effects (5-7, 12).
REFERENCES 1. Al-Mefty O, Teixeira A: Complex tumors of the glomus jugulare: criteria, treatment, and outcome. J Neurosurg 17:1356-1366, 2002.
2. Aziz K, Yu A, Chen D, Sekula R: Management of cranial nerve injuries. In: QuinonesHinojosa A, ed. Schmidek and Sweet Operative Neurosurgical Techniques: Indications, Methods and Results. Philadelphia: Saunders; 2012:2337-2338.
Deciding on an individualized management strategy requires a multidisciplinary approach. Imaging studies are performed, which include magnetic resonance imaging, computed tomography, and angiography. An extensive ear-nose-throat evaluation and swallowing evaluation is performed to detect and document lower cranial nerve dysfunction. Numerous factors are evaluated, which include size of the lesion, extent, and infiltration of the lesion, most likely pathology of the lesion, age of patient, previous radiation, medical comorbidities, involvement and patency of vascular structures, signs or symptoms of brainstem compression, cranial nerve deficits, and patient preference. For asymptomatic and small lesions that have been proven to enlarge on serial imaging, stereotactic radiosurgery provides an excellent option for stopping tumor growth. Lesions that are large and symptomatic as the result of mass effect tend to require surgical intervention. In this case, a judicious approach that uses nerve monitoring is implemented, and the specific approach is tailored according to the specific anatomical relationships of the lesion. In some cases an incomplete resection followed by stereotactic radiosurgery has proven to be a very well tolerated and safe approach. In others, multiple stages are performed at different settings. Since 1990 at our institution, during the course of roughly 370 posterior fossa and skull base tumors, we have dealt with most of these lesions via open microsurgical approaches. Lesions that originate in other locations and extend to involve the jugular foramen are in our system typically classified as foramen magnum meningiomas, CP angle lesions, etc. We have encountered 10 paragangliomas, 8 of which were successfully treated with stereotactic radiosurgery only; the other 2 required surgery. Nonglomus lesions isolated to the jugular foramen included 5 Schwannomas and 1 metastasis, all of which were treated with open surgery. In one case, a small residual was treated with radiosurgery. In our setting, our proclivity is to treat paragangliomas via radiosurgery, whereas other lesions are typically large enough to cause mass effect at the time of diagnosis, in which case surgery remains an essential part of management. The management of lesions involving the jugular foramen is complex and challenging, and treatment options need to be judiciously used and an individualized plan created for every patient’s unique disease. Although surgical intervention can offer immediate and absolute tumor control in some patients, it should only be entered into after careful consideration.
3. Cheesman A, Kelly A: Rehabilitation after treatment for jugular foramen lesions. Skull Base 1: 99-108, 2009. 4. Dahia PLM: Pheochromocytoma and paraganglioma pathogenesis: learning from genetic heterogeneity. Nat Rev Cancer 14:108-119, 2014. 5. Hasegawa T: Stereotactic radiosurgery for nonvestibular schwannomas. Neurosurg Clin N Am 24:531-542, 2013. 6. Huy P, Kania R, Duet M: Evolving concepts in the management of jugular paraganglioma: a
WORLD NEUROSURGERY 83 [2]: 164-166, FEBRUARY 2015
comparison of radiotherapy and surgery in 88 cases. Skull Base 1:83-91, 2009. 7. Lanzino G, Dumont AS, Lopes MB, Laws ER: Skull base chordomas: overview of disease, management options, and outcome. Neurosurg Focus 10:E12, 2001. 8. Liu JK, Gupta G, Christiano LD: Surgical management of tumors of the jugular foramen. In: Quinones-Hinojosa A, ed. Schmidek and Sweets Operative Neurosurgical Techniques: Indications, Methods and Results. 6th Ed. Philadelphia: Saunders; 2012:529-545.
www.WORLDNEUROSURGERY.org
165
PERSPECTIVES
9. Macdonald AJ, Salzman KL, Harnsberger HR, Gilbert E, Shelton C: Primary jugular foramen meningioma: imaging appearance and differentiating features. AJR Am J Roentgenol 182:373-377, 2004. 10. Di Maio S, Temkin N, Ramanathan D, Sekhar LN: Current comprehensive management of cranial base chordomas: 10-year meta-analysis of observational studies. J Neurosurg 115:1094-1105, 2011. 11. Megerian C, McKenna M, Nadol JB Jr: Nonparaganglioma jugular foramen lesions masquerading as glomus jugulare tumors. Otol Neurotol 16:94-98, 1995.
12. Ramina R, Maniglia JJ, Fernandes YB, Paschoal JR, Pfeilsticker LN, Neto MC, Borges G: Jugular foramen tumors: diagnosis and treatment. Neurosurg Focus 17:E5, 2004. 13. Rayappa C: Jugular foramen tumors. Otorhinolaryngol Clin 3:15-23, 2011. 14. Sanna M, De Donato G, Di Lella F: Nonvascular lesions of the jugular foramen: the gruppo otologico experience. Skull Base 1:57-74, 2009. 15. Vernet M: Syndrome du trou dechire posterieur (paralysie des IX, X, XII). Rev Neuro 34:117-148, 1918.
16. Vogl T, Bisdas S: Differential diagnosis of jugular foramen lesions. Skull Base 1(212):3-16, 2009.
Citation: World Neurosurg. (2015) 83, 2:164-166. http://dx.doi.org/10.1016/j.wneu.2014.11.008 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter Published by Elsevier Inc.
WORLD FEDERATION OF NEUROSURGICAL SOCIETIES Mission Statement To facilitate the personal association of neurological surgeons throughout the world. To aid in the exchange and dissemination of knowledge and ideas in the field of neurological surgery. To encourage research in neurological surgery and allied sciences. To address issues of neurosurgical demography. To address issues of Public Health. To implement, improve and promote the standards of neurosurgical care and training worldwide.
Membership Services (www.wfns.org) Teresa Chen Hsiao-Hui (Teresa) Chen Office Manager, WFNS Central Office World Federation of Neurosurgical Societies 5 Rue du Marché 1260 Nyon, Vaud, Switzerland Tel: +41 (0) 22 3624303 Fax: +41 (0) 22 3624352 Email: [email protected]
166
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.11.008
Diverse Pathologies of the Jugular Foramen Anil Nanda and Richard D. Murray
T
he posterior fossa presents a fascinatingly complex anatomical region that includes not only vital brainstem structures but also delicate cranial nerves in close proximity to major vascular structures. Once anatomical variation and tumor distortion are superimposed on this complex region, addressing lesions in this region presents unique challenges to skull base surgeons. Lesions of the jugular foramen are prime examples of these challenges. The sigmoid sinus and inferior petrosal sinus closely interact with the IXth, Xth, and XIth cranial nerves, all of which are located in a deep and medial corner of the posterior fossa, with the brainstem and rigid bony confines limiting access to this area. In a recent issue of WORLD NEUROSURGERY, Guinto et al. performed a comprehensive review of their 10-year experience in managing the unique pathology of this region. During this period, they operated on 70 patients with lesions involving the jugular foramen, 30 of which were nonglomic tumors. They then retrospectively studied these nonglomic tumors, which consisted of 18 schwannomas, 6 meningiomas, 5 chordomas, and 1 metastasis and documented their operative approach, surgical results, and preoperative imaging findings. All of their patients were actively symptomatic at time of presentation. As expected by the basic biology of the respective tumors, the patients with schwannoma and meningiomas tended to fare better in the long term, whereas patients with chordomas demonstrated a recurrent and relentless course, with 2 patients eventually succumbing to this disease. All of the authors’ patients were symptomatic at the time of presentation, and they elegantly highlight how preoperative imaging studies were useful in predicting the intraoperative pathology. Their surgical
Key words Approach - Infratemporal fossa - Jugular foramen - Nonglomic tumors - Skull base surgery -
164
www.SCIENCEDIRECT.com
outcomes speak to their extensive experience with dealing with such divergent pathologies that all involve the jugular foramen. Since the early 1900s when a variety of eponymous jugular foramen syndromes (Vernet, Collet-Sicard, etc) (2, 15) were first described, it has been well known that these constellations of neurologic signs can be caused by a variety of pathologies, ranging from benign to malignant tumors, ischemic and inflammatory events to cranial nerves, fractures of the skull base, and penetrating as well as blunt trauma. Neoplastic pathologies encountered in this region are diverse, with the most common being glomus jugulare tumors, which arise from paraganglia within the jugular adventitia (56%e77%) (11, 13, 16). These tend to have a characteristic growth pattern, being unencapsulated and infiltrating along tissue planes and pathways of least resistance, invading air cells, vascular lumens, skull base foramina, and the Eustachian tube (8, 16). Other pathologies, although less common, are nevertheless encountered. Nerve sheath tumors arise from the glossopharyngeal (IX), vagus (X), and accessory (XI) nerves (16). Meningiomas can originate either in the posterior fossa and grow to involve the jugular foramen or more rarely can have their epicenter in the jugular foramen itself and spread into the posterior fossa (16). They may have either a centrifugal growth pattern, growing in all directions from their epicenter, or they may exhibit an en plaque pattern, spreading along dural reflections (9, 16). Chordomas, although typically arising in the clivus and sphenooccipital synchondrosis, can grow eccentrically and involve the petrous bone and the jugular foramen (7, 10, 16). Other pathologies in this region may include various metastatic tumors, hemangiopericytoma, plasmacytoma, etc (11).
Department of Neurosurgery, Louisiana State University Health Sciences Center in Shreveport, Shreveport, Louisiana, USA To whom correspondence should be addressed: Anil Nanda, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 83, 2:164-166. http://dx.doi.org/10.1016/j.wneu.2014.11.008
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.11.008
PERSPECTIVES
Given the delicacy of structures in this region, the importance of cranial nerve efferent control over primitive functions such as swallowing and the prevention of aspiration, the relative lack of redundancy in these structures, coupled with the spatial crowding of this area, it is not surprising that interventions in this region tend to be fraught with risk. Lower cranial nerve dysfunction after surgery has a major impact on patient quality of life (3, 6, 8, 13, 14). Even relatively minor disturbances in swallowing function, although not always readily elicited during routine postoperative office visits, can have a very significant detriment to nutritional intake and quality of life (3). Pheochromocytomas and paragangliomas have the greatest degree of heritability of all human tumors, at approximately 40%. Approximately 40% of these carry a germline mutation in 1 of at least 12 genes. Within the last decade, a genetic driver event has been elucidated in roughly 50% of these lesions. These lesion play a unique role in the study of human cancer genetic mechanisms and have played a substantial role in our understanding of cancer biology (4). Concomitantly with the clarification of the different pathologies in this area, medical advances are ever improving our ability to address these pathologies. Magnetic resonance imaging can demonstrate extent of tumor infiltration, growth patterns, and spread. Computed tomography provides detailed bony anatomy and evaluation of the jugular foramen to demonstrate bony enlargement without destruction, especially in cases of schwannomas. Angiography is helpful in differentiating paragangliomas from other pathologies but also can help to demonstrate tumor blush and origin of feeding vessels, which can then be followed by judicious embolization. Balloon test occlusion studies help to predict whether occlusion of the petrous internal carotid artery would be tolerated. Nerve monitoring techniques help to warn surgeons of impending lower cranial nerve damage. Judicious use of endoscopy has evolved to enable smaller incisions and tailored trajectories. Microsurgical techniques and familiarity with skull base approaches has previously considered inoperable tumors to be managed successfully (1). Perhaps the most profound advance has been the role of radiotherapy in the management of these lesions. Proton beam therapy has established a strong role in the postsurgical management of skull base chordomas. Stereotactic radiosurgery has an ever-advancing role, not just as salvage option for tumor residuals postsurgery but also as a primary treatment modality for well-selected tumors, demonstrating a cessation of tumor growth with minimal side effects (5-7, 12).
REFERENCES 1. Al-Mefty O, Teixeira A: Complex tumors of the glomus jugulare: criteria, treatment, and outcome. J Neurosurg 17:1356-1366, 2002.
2. Aziz K, Yu A, Chen D, Sekula R: Management of cranial nerve injuries. In: QuinonesHinojosa A, ed. Schmidek and Sweet Operative Neurosurgical Techniques: Indications, Methods and Results. Philadelphia: Saunders; 2012:2337-2338.
Deciding on an individualized management strategy requires a multidisciplinary approach. Imaging studies are performed, which include magnetic resonance imaging, computed tomography, and angiography. An extensive ear-nose-throat evaluation and swallowing evaluation is performed to detect and document lower cranial nerve dysfunction. Numerous factors are evaluated, which include size of the lesion, extent, and infiltration of the lesion, most likely pathology of the lesion, age of patient, previous radiation, medical comorbidities, involvement and patency of vascular structures, signs or symptoms of brainstem compression, cranial nerve deficits, and patient preference. For asymptomatic and small lesions that have been proven to enlarge on serial imaging, stereotactic radiosurgery provides an excellent option for stopping tumor growth. Lesions that are large and symptomatic as the result of mass effect tend to require surgical intervention. In this case, a judicious approach that uses nerve monitoring is implemented, and the specific approach is tailored according to the specific anatomical relationships of the lesion. In some cases an incomplete resection followed by stereotactic radiosurgery has proven to be a very well tolerated and safe approach. In others, multiple stages are performed at different settings. Since 1990 at our institution, during the course of roughly 370 posterior fossa and skull base tumors, we have dealt with most of these lesions via open microsurgical approaches. Lesions that originate in other locations and extend to involve the jugular foramen are in our system typically classified as foramen magnum meningiomas, CP angle lesions, etc. We have encountered 10 paragangliomas, 8 of which were successfully treated with stereotactic radiosurgery only; the other 2 required surgery. Nonglomus lesions isolated to the jugular foramen included 5 Schwannomas and 1 metastasis, all of which were treated with open surgery. In one case, a small residual was treated with radiosurgery. In our setting, our proclivity is to treat paragangliomas via radiosurgery, whereas other lesions are typically large enough to cause mass effect at the time of diagnosis, in which case surgery remains an essential part of management. The management of lesions involving the jugular foramen is complex and challenging, and treatment options need to be judiciously used and an individualized plan created for every patient’s unique disease. Although surgical intervention can offer immediate and absolute tumor control in some patients, it should only be entered into after careful consideration.
3. Cheesman A, Kelly A: Rehabilitation after treatment for jugular foramen lesions. Skull Base 1: 99-108, 2009. 4. Dahia PLM: Pheochromocytoma and paraganglioma pathogenesis: learning from genetic heterogeneity. Nat Rev Cancer 14:108-119, 2014. 5. Hasegawa T: Stereotactic radiosurgery for nonvestibular schwannomas. Neurosurg Clin N Am 24:531-542, 2013. 6. Huy P, Kania R, Duet M: Evolving concepts in the management of jugular paraganglioma: a
WORLD NEUROSURGERY 83 [2]: 164-166, FEBRUARY 2015
comparison of radiotherapy and surgery in 88 cases. Skull Base 1:83-91, 2009. 7. Lanzino G, Dumont AS, Lopes MB, Laws ER: Skull base chordomas: overview of disease, management options, and outcome. Neurosurg Focus 10:E12, 2001. 8. Liu JK, Gupta G, Christiano LD: Surgical management of tumors of the jugular foramen. In: Quinones-Hinojosa A, ed. Schmidek and Sweets Operative Neurosurgical Techniques: Indications, Methods and Results. 6th Ed. Philadelphia: Saunders; 2012:529-545.
www.WORLDNEUROSURGERY.org
165
PERSPECTIVES
9. Macdonald AJ, Salzman KL, Harnsberger HR, Gilbert E, Shelton C: Primary jugular foramen meningioma: imaging appearance and differentiating features. AJR Am J Roentgenol 182:373-377, 2004. 10. Di Maio S, Temkin N, Ramanathan D, Sekhar LN: Current comprehensive management of cranial base chordomas: 10-year meta-analysis of observational studies. J Neurosurg 115:1094-1105, 2011. 11. Megerian C, McKenna M, Nadol JB Jr: Nonparaganglioma jugular foramen lesions masquerading as glomus jugulare tumors. Otol Neurotol 16:94-98, 1995.
12. Ramina R, Maniglia JJ, Fernandes YB, Paschoal JR, Pfeilsticker LN, Neto MC, Borges G: Jugular foramen tumors: diagnosis and treatment. Neurosurg Focus 17:E5, 2004. 13. Rayappa C: Jugular foramen tumors. Otorhinolaryngol Clin 3:15-23, 2011. 14. Sanna M, De Donato G, Di Lella F: Nonvascular lesions of the jugular foramen: the gruppo otologico experience. Skull Base 1:57-74, 2009. 15. Vernet M: Syndrome du trou dechire posterieur (paralysie des IX, X, XII). Rev Neuro 34:117-148, 1918.
16. Vogl T, Bisdas S: Differential diagnosis of jugular foramen lesions. Skull Base 1(212):3-16, 2009.
Citation: World Neurosurg. (2015) 83, 2:164-166. http://dx.doi.org/10.1016/j.wneu.2014.11.008 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter Published by Elsevier Inc.
WORLD FEDERATION OF NEUROSURGICAL SOCIETIES Mission Statement To facilitate the personal association of neurological surgeons throughout the world. To aid in the exchange and dissemination of knowledge and ideas in the field of neurological surgery. To encourage research in neurological surgery and allied sciences. To address issues of neurosurgical demography. To address issues of Public Health. To implement, improve and promote the standards of neurosurgical care and training worldwide.
Membership Services (www.wfns.org) Teresa Chen Hsiao-Hui (Teresa) Chen Office Manager, WFNS Central Office World Federation of Neurosurgical Societies 5 Rue du Marché 1260 Nyon, Vaud, Switzerland Tel: +41 (0) 22 3624303 Fax: +41 (0) 22 3624352 Email: [email protected]
166
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.11.008
