CC BY-NC-ND 4.0 · Asian J Neurosurg
DOI: 10.1055/s-0044-1787050
Review Article

Combined Deficit of the Four Lower Cranial Nerves also Known as the Syndrome of Collet-Sicard: A Systematic Review and Meta-analysis

1   Neurosurgery Department, Sainte-Anne Military Teaching Hospital, Toulon, France
2   Ecole du Val-de-Grâce, French Military Health Service Academy, Paris, France
› Author Affiliations
Funding None.

Abstract

Combined deficit of the four lower cranial nerves (CN IX, X, XI, and XII) was originally described by French physicians Collet (1915) and Sicard (1917) during World War I. To date though, this rare neurological clinical picture lacks systematic evidence regarding its epidemiology, clinical presentation, treatment strategies, and outcome. We conducted a systematic review and meta-analysis concerning Collet-Sicard syndrome (CSS) on Medline database in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. The research yielded 84 articles among which 73 individual case reports were eventually retained. Mean age was 53.7 (± 16) years old and the male-to-female ratio was 1.8/1. CSS was firstly caused by tumors (38.4%), following by vascular etiologies (28.8%), trauma (16.4%), and infection (6.8%), among others. Temporary enteral nutrition was required for 17 patients (23.3%). The four CN presented significant chances of complete or partial recovery: 52.1% for CN IX (p < 0.001), 46.6% for CN X and CN XII (p < 0.001), and 39.7% for CN XI (p = 0.002). Tumoral causes presented significantly lower chances of favorable CN recovery (7.1%) compared to infection (60%), vascular (52.4%), and trauma (41.7%) (p < 0.001). Older age (> 53 years old) was not associated with a dismal CN prognostic (p = 0.763). Most patients (71.2%) presented a favorable outcome (Glasgow Outcome Scale score ≥ 4). All the patients who died (6.8%) suffered from skull base tumors. CSS is a rare condition requiring prompt clinical and radiologic diagnostic and multidisciplinary management. Vascular or infectious-related CSS seem to present a rather good prognostic, closely followed by trauma, whereas tumoral-related CSS seem to suffer from a more dismal prognostic.



Publication History

Article published online:
13 May 2024

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  • References

  • 1 Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement. PLoS Med 2009; 6 (07) e1000097
  • 2 Al-Shabibi T, Hamdi H, Balaha A, Ghoraba Y, Kaya J-M. Delayed Collet-Sicard syndrome after internal carotid dissection and Jefferson fracture. Case report and review of literature. Surg Neurol Int 2021; 12: 374
  • 3 Amar JY, Ruta J, Bazer D, Bhattacharya A, Varadhachary AS. Collet-Sicard syndrome as the presentation of malignant pheochromocytoma. Neurohospitalist 2020; 10 (04) 320-321
  • 4 Arasawa T, Miyauchi H, Fujita E. et al. A case of rectal cancer with Collet-Sicard syndrome [in Japanese]. Gan To Kagaku Ryoho 2020; 47 (13) 2225-2226
  • 5 Barbiero FJ, Baehring JM, Fulbright RK, Becker KP. MRI findings in Collet-Sicard syndrome. Neurology 2017; 88 (08) 811
  • 6 Basu S, Nair N. Relapse of cervical cancer presenting as symptoms of Collet-Sicard syndrome with metastatic subcutaneous and adrenal deposits. Lancet Oncol 2006; 7 (07) 610
  • 7 Battaglia F, Martini L, Tannier C. Syndrome de Collet-Sicard après dissection carotidienne. Rev Neurol (Paris) 2009; 165 (6-7): 588-590
  • 8 Beucler N, Morvan J-B, Dagain A. An unusual posttraumatic dysphagia with special reference to cerebellopontine angle. JAMA Otolaryngol Head Neck Surg 2020; 146 (01) 73-74
  • 9 Bonda S, Tun KM, Asad S. A case of Collet-Sicard syndrome caused by otitis externa. Cureus [Internet] 2022. Accessed March 5, 2023 at: https://www.cureus.com/articles/95102-a-case-of-collet-sicard-syndrome-caused-by-otitis-externa
  • 10 Cabreira V, Lopes AC, Figueiredo R, Pinto MM. Collet-Sicard syndrome secondary to internal carotid artery dissection: a firing link. Neurohospitalist 2020; 10 (04) 322-323
  • 11 Chacon G, Alexandraki I, Palacio C. Collet-Sicard syndrome: an uncommon manifestation of metastatic prostate cancer. South Med J 2006; 99 (08) 898-899
  • 12 Climans SA, Melanson M, Desai JA. A case of Collet-Sicard syndrome caused by necrotizing otitis externa. Can J Neurol Sci 2013; 40 (02) 268-270
  • 13 Comacchio F, D'Eredità R, Poletto E, Poletti A, Marchiori C. Hemangiopericytoma of the skull base and Collet-Sicard syndrome: a case report. Ear Nose Throat J 1995; 74 (12) 845-847
  • 14 Connolly B, Turner C, DeVine J, Gerlinger T. Jefferson fracture resulting in Collet-Sicard syndrome. Spine 2000; 25 (03) 395-398
  • 15 Dey JK, Carlson ML. Jugular paraganglioma presenting with Collet-Sicard syndrome. Mayo Clin Proc 2019; 94 (09) 1832-1833
  • 16 Domenicucci M, Mancarella C, Dugoni ED, Ciappetta P, Paolo M. Post-traumatic Collet-Sicard syndrome: personal observation and review of the pertinent literature with clinical, radiologic and anatomic considerations. Eur Spine J 2015; 24 (04) 663-670
  • 17 Erben Y, Ghare MI, Patel A, Mojibian H, Matouk C. Collet-Sicard syndrome secondary to internal carotid artery pseudoaneurysm. J Vasc Surg 2018; 67 (05) 1596-1597
  • 18 Erol FS, Topsakal C, Kaplan M, Yildirim H, Ozveren MF. Collet-Sicard syndrome associated with occipital condyle fracture and epidural hematoma. Yonsei Med J 2007; 48 (01) 120-123
  • 19 Evan J, Johansen M, Akst LM. Dysphagia, dysphonia and a deviated tongue: diagnosing Collet-Sicard syndrome. BMJ Case Rep 2021; 14 (05) e243154
  • 20 Ganesh A, Assis Z, Fok D, Cairncross JG, Bal SS, Furtado S. Teaching NeuroImages: Collet-Sicard syndrome and hearing loss with glomus jugulotympanicum. Neurology 2019; 93 (14) e1408-e1409
  • 21 Garcia-Escrivà A, Pampliega Pérez A, Martín-Estefania C, Botella C. Schwannoma of the hypoglossal nerve presenting as a syndrome of Collet-Sicard[in Spanish]. Neurología 2005; 20 (06) 311-313
  • 22 Gutiérrez Ríos R, Castrillo Sanz A, Gil Polo C, Zamora García MI, Morollón Sánchez-Mateos N, Mendoza Rodríguez A. Collet-Sicard syndrome. Neurología 2015; 30 (02) 130-132
  • 23 Handley TPB, Miah MS, Majumdar S, Hussain SSM. Collet-Sicard syndrome from thrombosis of the sigmoid-jugular complex: a case report and review of the literature. Int J Otolaryngol 2010; 2010: 1-5
  • 24 Hashimoto T, Watanabe O, Takase M, Koniyama J, Kobota M. Collet-Sicard syndrome after minor head trauma. Neurosurgery 1988; 23 (03) 367-370
  • 25 Heckmann JG, Tomandl B, Duhm C, Stefan H, Neundörfer B. Collet-Sicard syndrome due to coiling and dissection of the internal carotid artery. Cerebrovasc Dis 2000; 10 (06) 487-488
  • 26 Hsu HP, Chen ST, Chen CJ, Ro LS. A case of Collet-Sicard syndrome associated with traumatic atlas fractures and congenital basilar invagination. J Neurol Neurosurg Psychiatry 2004; 75 (05) 782-784
  • 27 Kang K, Moon BG. Developmental abnormalities of the craniocervical junction resulting in Collet-Sicard syndrome. Spine J 2016; 16 (09) e635-e639
  • 28 Khalid S, Zaheer S, Khalid M, Zaheer S, Raghuwanshi RK. Collet-Sicard syndrome secondary to a large glomus jugulotympanicum. Ann Saudi Med 2013; 33 (04) 407-410
  • 29 Krishnan M, Balamurugan N, Thiruvarutchelvan K, Sivakumar S. Prostate cancer presenting as Collet-Sicard syndrome. J Assoc Physicians India 2019; 67 (08) 72
  • 30 Kwon HC, Cho DK, Jang YY, Lee SJ, Hyun JK, Kim TU. Collet-Sicard syndrome in a patient with Jefferson fracture. Ann Rehabil Med 2011; 35 (06) 934-938
  • 31 Larson WL, Beydoun A, Albers JW, Wald JJ. Collet-Sicard syndrome mimicking neuralgic amyotrophy. Muscle Nerve 1997; 20 (09) 1173-1177
  • 32 Lee J-S, Sy ED, Chang C-W, Chang S-S. Craniofacial gunshot injury resulting in pseudoaneurysm of the left internal maxillary artery and Collet-Sicard syndrome. J Craniofac Surg 2009; 20 (02) 568-571
  • 33 Lee SH, Lee ES, Yoon CH, Shin H, Lee CH. Collet-Sicard syndrome with hypoglossal nerve schwannoma: a case report. Ann Rehabil Med 2017; 41 (06) 1100-1104
  • 34 Lian C, Liu S, Li X, Du Z-H. The diagnosis process of Collet-Sicard syndrome caused by skull base fracture: a case report. Neurología (Engl Ed) 2021; 36 (08) 649-651
  • 35 Lin J, Zhou L, Hong D. Internal carotid artery aneurysm presenting as lower cranial nerve palsies. World Neurosurg 2023; 173: 23-24
  • 36 Low W-K, Lhu H-L. Skull base osteomyelitis from otitis media presenting as the Collet-Sicard syndrome. Case Rep Otolaryngol 2018; 2018: 1407417
  • 37 Lucato LT, Passos RBD, Campos CR, Conforto AB, McKinney AM. Neurological picture. Multidetector-row computed tomography in the diagnosis of Collet-Sicard syndrome. J Neurol Neurosurg Psychiatry 2008; 79 (05) 521-521
  • 38 Lucato LT, Passos RBD, Campos CR, Conforto AB, McKinney AM. Multidetector-row computed tomography in the diagnosis of Collet-Sicard syndrome. BMJ Case Rep 2009; 2009: bcr2007120972
  • 39 Maier S, Bajkó Z, Moţăţăianu A, Rusu S, Bălaşa R. Giant internal carotid artery aneurysm causing Collet-Sicard syndrome. Acta Neurol Belg 2017; 117 (01) 295-297
  • 40 Mnari W, Kilani M, Harrathi K, Maatouk M, Koubaa J, Golli M. An unusual etiology of posttraumatic Collet-Sicard Syndrome: a case report. Pan Afr Med J 2016; 23: 143
  • 41 Mohanty SK, Barrios M, Fishbone H, Khatib R. Irreversible injury of cranial nerves 9 through 12 (Collet-Sicard syndrome). Case report. J Neurosurg 1973; 38 (01) 86-88
  • 42 Mohr A, Ebert S, Knauth M. Spontane Dissektion der Arteria carotis interna mit ipsilateralem Collet-Sicard-Syndrom. Röfo Fortschr Geb Röntgenstr Neuen Bildgeb Verfahr 2006; 178 (04) 444-446
  • 43 Mutlu V, Ogul H. Magnetic resonance imaging features of Collet-Sicard syndrome associated with glomus jugulare paraganglioma. J Craniofac Surg 2019; 30 (06) e574-e576
  • 44 Nagata H, Sato S, Tanaka K. et al. Skull base metastasis of the breast cancer causing the Collet-Sicard syndrome–a case report (author's transl) [in Japanese]. No To Shinkei 1980; 32 (07) 695-700
  • 45 Neo S, Lee KE. Collet-Sicard syndrome: a rare but important presentation of internal jugular vein thrombosis. Pract Neurol 2017; 17 (01) 63-65
  • 46 Nowak DA, Linden R, Arnold P. et al. Case report: a complicated course of Collet-Sicard syndrome after internal carotid artery dissection and lenticulo-striatal artery infarction. Front Neurol 2022; 13: 939236
  • 47 Opie NJ, Ur-Rehman K, James GJ. A case of Collet-Sicard syndrome presenting to the oral and maxillofacial surgery department and a review of the literature. Br J Oral Maxillofac Surg 2010; 48 (04) e9-e11
  • 48 Otto M, Otto V, Götzinger R, Cordes P, Wessel K. Collet-Sicard's syndrome as a result of jugular vein thrombosis. J Neurol 2001; 248 (02) 143-144
  • 49 Oushy S, Graffeo CS, Perry A, Morris JM, Carlson ML, Van Gompel JJ. Collet-Sicard syndrome attributable to extramedullary plasmacytoma of the jugular foramen. World Neurosurg 2018; 110: 386-390
  • 50 Paparounas K, Gotsi A, Apostolou F, Akritidis N. Collet-Sicard syndrome disclosing glomus tumor of the skull base. Eur Neurol 2003; 49 (02) 103-105
  • 51 Petrović S, Grozdanović D, Kovačević P, Višnjić M, Petrović D. Collet Sicard syndrome as atypical presentation of neck fibrosarcoma: a case report. Bosn J Basic Med Sci 2011; 11 (02) 137-140
  • 52 Prashant R, Franks A. Collet-Sicard syndrome–a report and review. Lancet Oncol 2003; 4 (06) 376-377
  • 53 Prick MJ, Verhagen WI. The Collet-Sicard syndrome as a complication of cardiovascular surgery. J Neurol Neurosurg Psychiatry 1992; 55 (08) 741
  • 54 Rees JH, Valentine AR, Llewelyn JG. Spontaneous bilateral carotid and vertebral artery dissection presenting as a Collet-Sicard syndrome. Br J Radiol 1997; 70 (836) 856-858
  • 55 Saliou V, Ben Salem D, Ognard J. et al. A Collet-Sicard syndrome due to internal carotid artery dissection associated with cerebral amyloid angiopathy-related inflammation. SAGE Open Med Case Rep 2018; 6: 2050313  × 1877717
  • 56 Sánchez-Larsen A, Feria-Vilar I, Collado R, Segura T. Síndrome de Collet-Sicard metastásico. Neurología 2017; 32 (06) 399-401
  • 57 Satoh H, Nishiyama T, Horiguchi A, Nakashima J, Saito S, Murai M. A case of Collet-Sicard syndrome caused by skull base metastasis of prostate carcinoma [in Japanese]. Nippon Hinyokika Gakkai Zasshi 2000; 91 (06) 562-564
  • 58 Schuster NM, Karnezis S, Restrepo L. Teaching NeuroImages: granulomatosis with polyangiitis causing Collet-Sicard syndrome and refractory headache. Neurology 2015; 85 (23) e179-e180
  • 59 Sehitoğlu MA, Uneri C, Celikoyar MM, Tutkun A, Küllü S. Hemangiopericytoma as the cause of Collet-Sicard syndrome. ORL J Otorhinolaryngol Relat Spec 1990; 52 (02) 133-136
  • 60 Shahrvini B, Crawford K, Vahabzadeh-Hagh AM. Collet-Sicard syndrome after Jefferson fracture. Ear Nose Throat J 2022; 101 (07) NP273-NP275
  • 61 Sharma BS, Mahajan RK, Bhatia S, Khosla VK. Collet-Sicard syndrome after closed head injury. Clin Neurol Neurosurg 1994; 96 (02) 197-198
  • 62 Shi K, Zhang N, Li Y. et al. Be careful of Collet-Sicard syndrome: a rare result of carotid artery dissection. Headache 2022; 62 (03) 389-394
  • 63 Shine NP, O'Sullivan P. Collet-Sicard syndrome: a rare presentation of metastatic prostate adenocarcinoma. Auris Nasus Larynx 2005; 32 (03) 315-318
  • 64 Sibai TA, Ben-Galim PJ, Eicher SA, Reitman CA. Infectious Collet-Sicard syndrome in the differential diagnosis of cerebrovascular accident: a case of head-to-neck dissociation with skull-based osteomyelitis. Spine J 2009; 9 (04) e6-e10
  • 65 Simões J, Paiva S, Miguéis J, Miguéis A. A long styloid process and Collet-Sicard syndrome. Acta Otorrinolaringol Esp (Engl Ed) 2019; 70 (05) 310-311
  • 66 Smith R, Tassone P, Saada J. Collet-Sicard syndrome as a result of unilateral carotid artery dissection. BMJ Case Rep 2013; 2013: bcr2013200358-bcr2013200358
  • 67 Sokhi DS, Mithi CW, Ebrahim FA, Salyani A, Waa S, Riyat MS. Collet-Sicard syndrome due to concurrent extramedullary intracranial plasmacytoma and jugular venous sinus thrombosis in multiple myeloma. Clin Case Rep 2021; 9 (07) e04457
  • 68 Subha ST, Nordin A-J. Metastatic adenocarcinoma of temporal bone with Collet-Sicard syndrome. Iran J Otorhinolaryngol 2018; 30 (101) 361-364
  • 69 Tappin JA, Satchi G, Corless JA, Ashworth F. Multiple myeloma presenting as the Collet-Sicard syndrome. J Neurol Neurosurg Psychiatry 1996; 60 (01) 14-14
  • 70 Villatoro R, Romero C, Rueda A. Collet-Sicard syndrome as an initial presentation of prostate cancer: a case report. J Med Case Rep 2011; 5: 315
  • 71 Walker S, McCarron MO, Flynn PA, Watt M. Left internal carotid artery dissection presenting with headache, Collet-Sicard syndrome and sustained hypertension. Eur J Neurol 2003; 10 (06) 731-732
  • 72 Wani MA, Tandon PN, Banerji AK, Bhatia R. Collet-Sicard syndrome resulting from closed head injury: case report. J Trauma 1991; 31 (10) 1437-1439
  • 73 Willy PJ, McArdle P, Peters WJ. Surgical emphysema and Collet-Sicard syndrome after cryoblockade of the inferior alveolar nerve. Br J Oral Maxillofac Surg 2003; 41 (03) 190-192
  • 74 Zamudio Moya FJ, Sagarra Mur D, Pereira de Vicente M. Síndrome de Collet-Sicard secundario a infección por virus de la influenza A (H1N1). Neurología (Engl Ed) 2019; 34 (06) 418-419
  • 75 Chauvin F, Fischer L-P, Ferrandis J-J, Chauvin E, Gunepin F-X. Progress in surgery of limb's wounds during the Great War [in French]. Hist Sci Med 2002; 36 (02) 157-173
  • 76 Koehler U, Conradt R. The inventor of the “Triage”: Dominique-Jean Larrey (1766-1842), Napoleon's Chief Military Doctor [in German]. Pneumologie 2022; 76 (05) 365-369
  • 77 Vernet. RIMBAUD. Syndrome condylo-déchiré postérieur. Société Med Chir; 1918
  • 78 Collet FJ. Sur un nouveau syndrome paralytique pharyngo-laryngé par blessure de guerre (hémiplégie glosso-laryngo-scapulo-pharyngée). Lyon Med 1915; •••: 121-129
  • 79 Sicard A. Syndrome du carrefour condylo-déchiré posterieur (type pur de paralysie des quatre derniers nerfs crâniens). Mars Med 1917; •••: 385-397
  • 80 Villaret. Le syndrome nerveux de l'espace rétro-parotidien postérieur. Rev Neurol (Paris); 1916
  • 81 Ayeni SA, Ohata K, Tanaka K, Hakuba A. The microsurgical anatomy of the jugular foramen. J Neurosurg 1995; 83 (05) 903-909
  • 82 Tummala RP, Coscarella E, Morcos JJ. Surgical anatomy of the jugular foramen. Oper Techniq Neurosurg 2005; 8: 2-5
  • 83 Beucler N, Boissonneau S, Ruf A, Fuentes S, Carron R, Dufour H. Crossed brainstem syndrome revealing bleeding brainstem cavernous malformation: an illustrative case. BMC Neurol 2021; 21 (01) 204
  • 84 Jorquera Moya M, Merino Menéndez S, Porta Etessam J, Escribano Vera J, Yus Fuertes M. Cranial nerve disorders: clinical manifestations and topography. Radiología (Engl Ed) 2019; 61 (02) 99-123
  • 85 Karnofsky DA, Abelmann WH, Craver LF, Burchenal JH. The use of the nitrogen mustards in the palliative treatment of carcinoma. With particular reference to bronchogenic carcinoma. Cancer 1948; 1: 634-656
  • 86 Sperduto PW, Kased N, Roberge D. et al. Summary report on the graded prognostic assessment: an accurate and facile diagnosis-specific tool to estimate survival for patients with brain metastases. J Clin Oncol 2012; 30 (04) 419-425
  • 87 Beucler N, Haikal C, Sellier A, May A, Meyer M, Fuentes S. Far-lateral approach for foramen magnum meningioma: an anatomical study with special reference to bulbopontine junction. Asian J Neurosurg 2022; 17 (04) 656-660
  • 88 Bruneau M, George B. Foramen magnum meningiomas: detailed surgical approaches and technical aspects at Lariboisière Hospital and review of the literature. Neurosurg Rev 2008; 31 (01) 19-32 , discussion 32–33
  • 89 Chibbaro S, Mirone G, Makiese O, Bresson D, George B. Dumbbell-shaped jugular foramen schwannomas: surgical management, outcome and complications on a series of 16 patients. Neurosurg Rev 2009; 32 (02) 151-159 , discussion 159
  • 90 Makiese O, Chibbaro S, Marsella M, Tran Ba Huy P, George B. Jugular foramen paragangliomas: management, outcome and avoidance of complications in a series of 75 cases. Neurosurg Rev 2012; 35 (02) 185-194 , discussion 194
  • 91 Johnson J, Barani IJ. Radiotherapy for malignant tumors of the skull base. Neurosurg Clin N Am 2013; 24 (01) 125-135
  • 92 Anderson PA, Montesano PX. Morphology and treatment of occipital condyle fractures. Spine 1988; 13 (07) 731-736
  • 93 Hu Y, Yuan Z-S, Kepler CK, Dong W-X, Sun X-Y, Zhang J. Comparison of occipitocervical and atlantoaxial fusion in treatment of unstable Jefferson fractures. Indian J Orthop 2017; 51 (01) 28-35
  • 94 Noble ER, Smoker WR. The forgotten condyle: the appearance, morphology, and classification of occipital condyle fractures. AJNR Am J Neuroradiol 1996; 17 (03) 507-513
  • 95 Bontinis V, Antonopoulos CN, Bontinis A. et al. A systematic review and meta-analysis of carotid artery stenting for the treatment of cervical carotid artery dissection. Eur J Vasc Endovasc Surg 2022; 64 (04) 299-308
  • 96 Sultan S, Hynes N, Acharya Y, Kavanagh E, Jordan F. Systematic review of the effectiveness of carotid surgery and endovascular carotid stenting versus best medical treatment in managing symptomatic acute carotid artery dissection. Ann Transl Med 2021; 9 (14) 1212
  • 97 Nepal G, Kharel S, Bhagat R. et al. Safety and efficacy of Direct Oral Anticoagulants in cerebral venous thrombosis: a meta-analysis. Acta Neurol Scand 2022; 145 (01) 10-23
  • 98 Ramina R, Maniglia JJ, Fernandes YB, Paschoal JR, Pfeilsticker LN, Coelho Neto M. Tumors of the jugular foramen: diagnosis and management. Neurosurgery 2005; 57 (1, Suppl): 59-68