Abstract
The exact pathogenesis of syringomyelia associated with Chiari type 1 malformation is unknown, although a number of authors have reported their theories of syrinx formation. The purpose of this review is to understand evidences based on the known theories and to create a new hypothesis of the pathogenesis. We critically review the literatures on clinicopathological, radiological, and clinical features of this disorder. The previously proposed theories mainly focused on the driven mechanisms of the cerebrospinal fluid (CSF) into the spinal cord. They did not fully explain radiological features or effects of surgical treatment such as shunting procedures. Common findings of the syrinx in clinicopathological studies were the communication with the central canal and extracanalicular extension to the posterior gray matter. Most of the magnetic resonance imaging studies demonstrated blockade and alternated CSF dynamics at the foramen magnum, but failed to show direct communication of the syrinx with the CSF spaces. Pressure studies revealed almost identical intrasyrinx pressure to the subarachnoid space and decreased compliance of the spinal CSF space. Recent imaging studies suggest that the extracellular fluid accumulation may play an important role. The review of evidences promotes a new hypothesis of syrinx formation. Decreased absorption mechanisms of the extracellular fluid may underlie the pathogenesis of syringomyelia. Reduced compliance of the posterior spinal veins associated with the decreased compliance of the spinal subarachnoid space will result in disturbed absorption of the extracellular fluid through the intramedullary venous channels and formation of syringomyelia.
Similar content being viewed by others
References
Aboulezz AO, Sartor K, Geyer CA, Gado MH (1985) Position of cerebellar tonsils in the normal population and in patients with Chiari malformation: a quantitative approach with MR imaging. J Comput Assist Tomogr 9:1033–1036
Akiyama Y, Koyanagi I, Yoshifuji K, Murakami T, Baba T, Minamida Y, Nonaka T, Houkin K (2008) Interstitial spinal-cord oedema in syringomyelia associated with Chiari type 1 malformations. J Neurol Neurosurg Psychiatry 79:1153–1158
Alperin N, Sivaramakrishnan A, Lichtor T (2005) Magnetic resonance imaging-based measurements of cerebrospinal fluid and blood flow as indicators of intracranial compliance in patients with Chiari malformation. J Neurosurg 103:46–52
Alzate JC, Kothbauer KF, Jallo GI, Epstein FJ (2001) Treatment of Chiari I malformation in patients with and without syringomyelia: a consecutive series of 66 cases. Neurosurg Focus 11:E3
Anderson RC, Dowling KC, Feldstein NA, Emerson RG (2003) Chiari I malformation: potential role for intraoperative electrophysiologic monitoring. J Clin Neurophysiol 20:65–72
Armonda RA, Citrin CM, Foley KT, Ellenbogen RG (1994) Quantitative cine-mode magnetic resonance imaging of Chiari I malformations: an analysis of cerebrospinal fluid dynamics. Neurosurgery 35:214–223
Arora P, Behari S, Banerji D, Chhabra DK, Jain VK (2004) Factors influencing the outcome in symptomatic Chiari I malformation. Neurol India 52:470–474
Arruda JA, Costa CM, Tella OI Jr (2004) Results of the treatment of syringomyelia associated with Chiari malformation: analysis of 60 cases. Arq Neuropsiquiatr 62:237–244
Asgari S, Engelhorn T, Bschor M, Sandalcioglu IE, Stolke D (2003) Surgical prognosis in hindbrain related syringomyelia. Acta Neurol Scand 107:12–21
Attal N, Parker F, Tadi_ M, Aghakani N, Bouhassira D (2004) Effects of surgery on the sensory deficits of syringomyelia and predictors of outcome: a long term prospective study. J Neurol Neurosurg Psychiatry 75:1025–1030
Attenello FJ, McGirt MJ, Gathinji M, Datoo G, Atiba A, Weingart J, Carson B, Jallo GI (2008) Outcome of Chiari-associated syringomyelia after hindbrain decompression in children: analysis of 49 consecutive cases. Neurosurgery 62:1307–1313
Attenello FJ, McGirt MJ, Garcés-Ambrossi GL, Chaichana KL, Carson B, Jallo GI (2009) Suboccipital decompression for Chiari I malformation: outcome comparison of duraplasty with expanded polytetrafluoroethylene dural substitute versus pericranial autograft. Childs Nerv Syst 25:183–190
Aubin ML, Vignaud J, Jardin C, Bar D (1981) Computed tomography in 75 clinical cases of syringomyelia. AJNR 2:199–204
Aydin S, Hanimoglu H, Tanriverdi T, Yentur E, Kaynar MY (2005) Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surg Neurol 64:237–241
Badie B, Mendoza D, Batzdorf U (1995) Posterior fossa volume and response to suboccipital decompression in patients with Chiari I malformation. Neurosurgery 37:214–218
Ball MJ, Dayan AD (1972) Pathogenesis of syringomyelia. Lancet 2:799–801
Barbaro NM, Wilson CB, Gutin PH, Edwards MS (1984) Surgical treatment of syringomyelia. Favorable results with syringoperitoneal shunting. J Neurosurg 61:531–538
Barkovich AJ, Wippold FJ, Sherman JL, Citrin CM (1986) Significance of cerebellar tonsillar position on MR. AJNR 7:795–799
Batzdorf U, Klekamp J, Johnson JP (1998) A critical appraisal of syrinx cavity shunting procedures. J Neurosurg 89:382–388
Beuls EA, Vandersteen MA, Vanormelingen LM, Adriaensens PJ, Freling G, Herpers MJ, Gelan JM (1996) Deformation of the cervicomedullary junction and spinal cord in a surgically treated adult Chiari I hindbrain hernia associated with syringomyelia: a magnetic resonance microscopic and neuropathological study. Case report. J Neurosurg 85:701–708
Bhadelia RA, Bogdan AR, Wolpert SM, Lev S, Appignani BA, Heilman CB (1995) Cerebrospinal fluid flow waveforms: analysis in patients with Chiari I malformation by means of gated phase-contrast MR imaging velocity measurements. Radiology 196:195–202
Bhangoo R, Sgouros S (2006) Scoliosis in children with Chiari I-related syringomyelia. Childs Nerv Syst 22:1154–1157
Bidziński J (1988) Pathological findings in suboccipital decompression in 63 patients with syringomyelia. Acta Neurochir Suppl (Wien) 43:26–28
Blagodatsky MD, Larionov SN, Manohin PA, Shanturov VA, Gladyshev YuV (1993) Surgical treatment of “hindbrain related” syringomyelia: new data for pathogenesis. Acta Neurochir (Wien) 124:82–85
Blagodatsky MD, Larionov SN, Alexandrov YA, Velm AI (1999) Surgical treatment of Chiari I malformation with or without syringomyelia. Acta Neurochir (Wien) 141:963–968
Bonafé A, Manelfe C, Espagno J, Guiraud B, Rascol A (1980) Evaluation of syringomyelia with metrizamide computed tomographic myelography. J Comput Assist Tomogr 4:797–802
Bosley TM, Cohen DA, Schatz NJ, Zimmerman RA, Bilaniuk LT, Savino PJ, Sergott RS (1985) Comparison of metrizamide computed tomography and magnetic resonance imaging in the evaluation of lesions at the cervicomedullary junction. Neurology 35:485–492
Brugieres P, Idy-Peretti I, Iffenecker C, Parker F, Jolivet O, Hurth M, Gaston A, Bittoun J (2000) CSF flow measurement in syringomyelia. AJNR 21:1785–1792
Cahan LD, Bentson JR (1982) Considerations in the diagnosis and treatment of syringomyelia and the Chiari malformation. J Neurosurg 57:24–31
Caldarelli M, Novegno F, Vassimi L, Romani R, Tamburrini G, Di Rocco C (2007) The role of limited posterior fossa craniectomy in the surgical treatment of Chiari malformation Type I: experience with a pediatric series. J Neurosurg 106(3 Suppl):187–195
Calliauw L, Dehaene I (1977) The surgical risk in the treatment of Arnold Chiari malformations. Acta Neurochir (Wien) 39:173–179
Danish SF, Samdani A, Hanna A, Storm P, Sutton L (2006) Experience with acellular human dura and bovine collagen matrix for duraplasty after posterior fossa decompression for Chiari malformations. J Neurosurg 104(1 Suppl):16–20
da Silva JA, Holanda MM (2003) Basilar impression, Chiari malformation and syringomyelia: a retrospective study of 53 surgically treated patients. Arq Neuropsiquiatr 61:368–375
Davis CH, Symon L (1989) Mechanisms and treatment in post-traumatic syringomyelia. Br J Neurosurg 3:669–674
DeLaPaz RL, Brady TJ, Buonanno FS, New PF, Kistler JP, McGinnis BD, Pykett IL, Taveras JM (1983) Nuclear magnetic resonance (NMR) imaging of Arnold-Chiari type I malformation with hydromyelia. J Comput Assist Tomogr 7:126–129
Depreitere B, Van Calenbergh F, van Loon J, Goffin J, Plets C (2000) Posterior fossa decompression in syringomyelia associated with a Chiari malformation: a retrospective analysis of 22 patients. Clin Neurol Neurosurg 102:91–96
Di Lorenzo N, Palma L, Palatinsky E, Fortuna A (1995) “Conservative” cranio-cervical decompression in the treatment of syringomyelia-Chiari I complex. A prospective study of 20 adult cases. Spine 20:2479–2483
Dolar MT, Haughton VM, Iskandar BJ, Quigley M (2004) Effect of craniocervical decompression on peak CSF velocities in symptomatic patients with Chiari I malformation. AJNR 25:142–145
Dones J, De Jesus O, Colen CB, Toledo MM, Delgado M (2003) Clinical outcomes in patients with Chiari I malformation: a review of 27 cases. Surg Neurol 60:142–148
Dubois PJ, Drayer BP, Sage M, Osborne D, Heinz ER (1981) Intramedullary penetrance of metrizamide in the dog spinal cord. AJNR 2:313–317
Duddy MJ, Williams B (1991) Hindbrain migration after decompression for hindbrain hernia: a quantitative assessment using MRI. Br J Neurosurg 5:141–152
Durham SR, Fjeld-Olenec K (2008) Comparison of posterior fossa decompression with and without duraplasty for the surgical treatment of Chiari malformation Type I in pediatric patients: a meta-analysis. J Neurosurg Pediatr 2:42–49
Dyste GN, Menezes AH, VanGilder JC (1989) Symptomatic Chiari malformations. An analysis of presentation, management, and long-term outcome. J Neurosurg 71:159–168
Ekholm SE, Foley M, Kido DK, Morris TW (1984) Lumbar myelography with metrizamide in rabbits. An investigation of contrast media penetration and resorption. Acta Radiol Diagn (Stockh) 25:517–522
Eldevik OP (1983) Elimination of metrizamide from the spinal subarachnoid space: a study of patients with abolished intracranial circulation. AJNR 4:585–587
Ellertsson AB, Greitz T (1970) The distending force in the production of communicating syringomyelia. Lancet 1(7658):1234
Elster AD, Chen MY (1992) Chiari I malformations: clinical and radiologic reappraisal. Radiology 183:347–353
Ergün R, Akdemir G, Gezici AR, Tezel K, Beskonakli E, Erg_ng_r F, Taskin Y (2000) Surgical management of syringomyelia-Chiari complex. Eur Spine J 9:553–557
Falcone S, Quencer RM, Green BA, Patchen SJ, Post MJ (1994) Progressive posttraumatic myelomalacic myelopathy: imaging and clinical features. AJNR Am J Neuroradiol 15:747–754
Fischbein NJ, Dillon WP, Cobbs C, Weinstein PR (1999) The “presyrinx” state: a reversible myelopathic condition that may precede syringomyelia. AJNR Am J Neuroradiol 20:7–20
Forbes WS, Isherwood I (1978) Computed tomography in syringomyelia and the associated Arnold-Chiari type I malformation. Neuroradiology 27:73–78
Fujii K, Natori Y, Nakagaki H, Fukui M (1991) Management of syringomyelia associated with Chiari malformation: comparative study of syrinx size and symptoms by magnetic resonance imaging. Surg Neurol 36:281–285
Furuya K, Sano K, Segawa H, Ide K, Yoneyama H (1998) Symptomatic tonsillar ectopia. J Neurol Neurosurg Psychiatry 64:221–226
Galarza M, Sood S, Ham S (2007) Relevance of surgical strategies for the management of pediatric Chiari type I malformation. Childs Nerv Syst 23:691–696
Gambardella G, Caruso G, Caffo M, Germanò A, La Rosa G, Tomasello F (1998) Transverse microincisions of the outer layer of the dura mater combined with foramen magnum decompression as treatment for syringomyelia with Chiari I malformation. Acta Neurochir (Wien) 140:134–139
Garcìa-Uria J, Leunda G, Carrillo R, Bravo G (1981) Syringomyelia: long-term results after posterior fossa decompression. J Neurosurg 54:380–383
Gardner WJ, Goodall RJ (1950) The surgical treatment of Arnold-Chiari malformation in adults. An explanation of its mechanism and importance of encephalography in diagnosis. J Neurosurg 7:199–206
Gardner WJ, Ange J (1958) The mechanism of syringomyelia and its surgical correction. Clin Neurosurg 6:131–140
Gardner WJ (1965) Hydrodynamic mechanism of syringomyelia: its relationship to myelocele. J Neurol Neurosurg Psychiatry 28:247–259
Ganong WF (1985) Dynamics of blood flow and lymph flow. In: Review of Medical Physiology, 12th edn. Lange Medical Publications, Maruzen Co, Tokyo, pp 470–484
Genitori L, Peretta P, Nurisso C, Macinante L, Mussa F (2000) Chiari type I anomalies in children and adolescents: minimally invasive management in a series of 53 cases. Childs Nerv Syst 16:707–718
Gillilan LA (1970) Veins of the spinal cord. Anatomic details; suggested clinical applications. Neurology 20:860–868
Goel A, Bhatjiwale M, Desai K (1998) Basilar invagination: a study based on 190 surgically treated patients. J Neurosurg 88:962–968
Goel A, Desai K (2000) Surgery for syringomyelia: an analysis based on 163 surgical cases. Acta Neurochir (Wien) 142:293–302
Goh S, Bottrell CL, Aiken AH, Dillon WP, Wu YW (2008) Presyrinx in children with Chiari malformations. Neurology 71:351–356
Golman K, Wiik I, Salvesen S (1979) Absorption of a non-ionic contrast agent from cerebrospinal fluid to blood. Neuroradiology 18:227–233
Grabb PA, Mapstone TB, Oakes WJ (1999) Ventral brain stem compression in pediatric and young adult patients with Chiari I malformations. Neurosurgery 44:520–528
Greenlee JD, Donovan KA, Hasan DM, Menezes AH (2002) Chiari I malformation in the very young child: the spectrum of presentations and experience in 31 children under age 6 years. Pediatrics 110:1212–1219
Greitz D, Ericson K, Flodmark O (1999) Pathogenesis and mechanics of spinal cysts. A new hypothesis based on magnetic resonance stdies of cerebrospinal fluid dynamics. Int J Neuroradiol 5:61–78
Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–264
Guo F, Wang M, Long J, Wang H, Sun H, Yang B, Song L (2007) Surgical management of Chiari malformation: analysis of 128 cases. Pediatr Neurosurg 43:375–381
Guyotat J, Bret P, Jouanneau E, Ricci AC, Lapras C (1998) Syringomyelia associated with type I Chiari malformation. A 21-year retrospective study on 75 cases treated by foramen magnum decompression with a special emphasis on the value of tonsils resection. Acta Neurochir (Wien) 140:745–754
Häckel M, Benes V, Mohapl M (2001) Simultaneous cerebral and spinal fluid pressure recordings in surgical indications of the Chiari malformation without myelodysplasia. Acta Neurochir (Wien) 143:909–918
Haughton VM, Korosec FR, Medow JE, Dolar MT, Iskandar BJ (2003) Peak systolic and diastolic CSF velocity in the foramen magnum in adult patients with Chiari I malformations and in normal control participants. AJNR 24:169–176
Hayhurst C, Richards O, Zaki H, Findlay G, Pigott TJ (2008) Hindbrain decompression for Chiari-syringomyelia complex: an outcome analysis comparing surgical techniques. Br J Neurosurg 22:86–91
Heiss JD, Patronas N, DeVroom HL, Shawker T, Ennis R, Kammerer W, Eidsath A, Talbot T, Morris J, Eskioglu E, Oldfield EH (1999) Elucidating the pathophysiology of syringomyelia. J Neurosurg 91:553–562
Hida K, Iwasaki Y, Koyanagi I, Sawamura Y, Abe H (1995) Surgical indication and results of foramen magnum decompression versus syringosubarachnoid shunting for syringomyelia associated with Chiari I malformation. Neurosurgery 37:673–679
Hida K, Iwasaki Y, Koyanagi I, Abe H (1999) Pediatric syringomyelia with chiari malformation: its clinical characteristics and surgical outcomes. Surg Neurol 51:383–391
Hida K, Iwasaki Y (2001) Syringosubarachnoid shunt for syringomyelia associated with Chiari I malformation. Neurosurg Focus 11:E7
Hinokuma K, Ohama E, Oyanagi K, Kakita A, Kawai K, Ikuta F (1992) Syringomyelia. A neuropathological study of 18 autopsy cases. Acta Pathol Jpn 42:25–34
Hoffman CE, Souweidane MM (2008) Cerebrospinal fluid-related complications with autologous duraplasty and arachnoid sparing in type I Chiari malformation. Neurosurgery 62(3 Suppl 1):156–161
Hoffman HJ, Neill J, Crone KR, Hendrick EB, Humphreys RP (1987) Hydrosyringomyelia and its management in childhood. Neurosurgery 21:347–351
Hofmann E, Warmuth-Metz M, Bendszus M, Solymosi L (2000) Phase-contrast MR imaging of the cervical CSF and spinal cord: volumetric motion analysis in patients with Chiari I malformation. AJNR 21:151–158
Holly LT, Batzdorf U (2001) Management of cerebellar ptosis following craniovertebral decompression for Chiari I malformation. J Neurosurg 94:21–26
Holtas S, Morris TW, Ekholm SE, Isaac L, Fonte D (1986) Penetration of subarachnoid contrast medium into rabbit spinal cord. Comparison between metrizamide and iohexol. Invest Radiol 21:151–155
Ikata T, Masaki K, Kashiwaguchi S (1988) Clinical and experimental studies on permeability of tracers in normal spinal cord and syringomyelia. Spine 13:737–741
Ikushima I, Korogi Y, Hirai T, Yamashita Y (2007) High-resolution constructive interference in a steady state imaging of cervicothoracic adhesive arachnoiditis. J Comput Assist Tomogr 31:143–147
Isherwood I, Fawcitt RA, St Clair Forbes W, Nettle JR, Pullan BR (1977) Computer tomography of the spinal canal using metrizamide. Acta Radiol Suppl 355:299–305
Iskandar BJ, Hedlund GL, Grabb PA, Oakes WJ (1998) The resolution of syringohydromyelia without hindbrain herniation after posterior fossa decompression. J Neurosurg 89:212–216
Iskandar BJ, Quigley M, Haughton VM (2004) Foramen magnum cerebrospinal fluid flow characteristics in children with Chiari I malformation before and after craniocervical decompression. J Neurosurg 101(2 Suppl):169–178
Isu T, Iwasaki Y, Sasaki H, Abe H, Tashiro K, Nakamura N (1987) An autopsy case of syringomyelia associated with Chiari malformation and basilar impression [in Japanese]. No Shinkei Geka 15:671–675
Isu T, Iwasaki Y, Akino M, Abe H (1990) Syringo-subarachnoid shunt for syringomyelia associated with Chiari malformation (type 1). Acta Neurochir (Wien) 107:152–160
Isu T, Iwasaki Y, Akino M, Abe H (1990) Hydrosyringomyelia associated with a Chiari I malformation in children and adolescents. Neurosurgery 26:591–597
Isu T, Sasaki H, Takamura H, Kobayashi N (1993) Foramen magnum decompression with removal of the outer layer of the dura as treatment for syringomyelia occurring with Chiari I malformation. Neurosurgery 33:844–850
Iwasaki Y, Abe H, Isu T, Miyasaka K (1985) CT myelography with intramedullary enhancement in cervical spondylosis. J Neurosurg 63:363–366
Iwasaki Y, Koyanagi I, Hida K, Abe H (1999) Syringo-subarachnoid shunt for syringomyelia using partial hemilaminectomy. Br J Neurosurg 13:41–45
Iwasaki Y, Hida K, Koyanagi I, Abe H (2000) Reevaluation of syringosubarachnoid shunt for syringomyelia with Chiari malformation. Neurosurgery 46:407–413
James HE, Brant A (2002) Treatment of the Chiari malformation with bone decompression without durotomy in children and young adults. Childs Nerv Syst 18:202–206
Jinkins JR, Bashir R, Al-Mefty O, Al-Kawi MZ, Fox JL (1986) Cystic necrosis of the spinal cord in compressive cervical myelopathy: demonstration by iopamidol CT-myelography. AJR 147:767–775
Kan S, Fox AJ, Vinuela F, Debrun G (1983) Spinal cord size in syringomyelia: change with position on metrizamide myelography. Radiology 146:409–414
Kan S, Fox AJ, Vinuela F (1985) Delayed metrizamide CT enhancement of syringomyelia: postoperative observations. AJNR 6:613–616
Karagoz F, Izgi N, Kapijcijoglu Sencer S (2002) Morphometric measurements of the cranium in patients with Chiari type I malformation and comparison with the normal population. Acta Neurochir (Wien) 144:165–171
Klekamp J, Batzdorf U, Samii M, Bothe HW (1996) The surgical treatment of Chiari I malformation. Acta Neurochir (Wien) 138:788–801
Klekamp J (2002) The pathophysiology of syringomyelia—historical overview and current concept. Acta Neurochir (Wien) 144:649–664
Koc K, Anik Y, Anik I, Cabuk B, Ceylan S (2007) Chiari 1 malformation with syringomyelia: correlation of phase-contrast cine MR imaging and outcome. Turk Neurosurg 17:183–192
Koyanagi I, Iwasaki Y, Hida K, Houkin K (2005) Clinical features and pathomechanisms of syringomyelia associated with spinal arachnoiditis. Surg Neurol 63:350–355
Krieger MD, McComb JG, Levy ML (1999) Toward a simpler surgical management of Chiari I malformation in a pediatric population. Pediatr Neurosurg 30:113–121
Kumar R, Kalra SK, Vaid VK, Mahapatra AK (2008) Chiari I malformation: surgical experience over a decade of management. Br J Neurosurg 22:409–414
Kyoshima K, Kuroyanagi T, Oya F, Kamijo Y, El-Noamany H, Kobayashi S (2002) Syringomyelia without hindbrain herniation: tight cisterna magna. Report of four cases and a review of the literature. J Neurosurg 96(2 Suppl):239–249
Kyoshima K, Kuroyanagi T, Toriyama T, Takizawa T, Hirooka Y, Miyama H, Tanabe A, Oikawa S (2004) Surgical experience of syringomyelia with reference to the findings of magnetic resonance imaging. J Clin Neurosci 11:273–279
LaMasters DL, Watanabe TJ, Chambers EF, Norman D, Newton TH (1982) Multiplanar metrizamide-enhanced CT imaging of the foramen magnum. AJNR 3:485–494
Lazareff JA, Galarza M, Gravori T, Spinks TJ (2002) Tonsillectomy without craniectomy for the management of infantile Chiari I malformation. J Neurosurg 97:1018–1022
Lee TT, Arias JM, Andrus HL, Quencer RM, Falcone SF, Green BA (1997) Progressive posttraumatic myelomalacic myelopathy: treatment with untethering and expansive duraplasty. J Neurosurg 86:624–628
Lesoin F, Petit H, Thomas CE 3rd, Viaud C, Baleriaux D, Jomin M (1986) Use of the syringoperitoneal shunt in the treatment of syringomyelia. Surg Neurol 25:131–136
Levine DN (2004) The pathogenesis of syringomyelia associated with lesions at the foramen magnum: a critical review of existing theories and proposal of a new hypothesis. J Neurol Sci 220:3–21
Levy WJ, Mason L, Hahn JF (1983) Chiari malformation presenting in adults: a surgical experience in 127 cases. Neurosurgery 12:377–390
Li KC, Chui MC (1987) Conventional and CT metrizamide myelography in Arnold-Chiari I malformation and syringomyelia. AJNR 8:11–17
Limonadi FM, Selden NR (2004) Dura-splitting decompression of the craniocervical junction: reduced operative time, hospital stay, and cost with equivalent early outcome. J Neurosurg 101(2 Suppl):184–188
Lipson AC, Ellenbogen RG, Avellino AM (2008) Radiographic formation and progression of cervical syringomyelia in a child with untreated Chiari I malformation. Pediatr Neurosurg 44:221–223
Liu B, Wang ZY, Xie JC, Han HB, Pei XL (2007) Cerebrospinal fluid dynamics in Chiari malformation associated with syringomyelia. Chin Med J (Engl) 120:219–223
Logue V, Edwards MR (1981) Syringomyelia and its surgical treatment—an analysis of 75 patients. J Neurol Neurosurg Psychiatry 44:273–284
Lund-Johansen M, Wester K (1997) Syringomyelia treated with a nonvalved syringoperitoneal shunt: a follow-up study. Neurosurgery 41:858–865
MacDonald RL, Findlay JM, Tator CH (1988) Microcystic spinal cord degeneration causing posttraumatic myelopathy. Report of two cases. J Neurosurg 68:466–471
Mariani C, Cislaghi MG, Barbieri S, Filizzolo F, Di Palma F, Farina E, D'Aliberti G, Scarlato G (1991) The natural history and results of surgery in 50 cases of syringomyelia. J Neurol 238:433–438
Masur H, Oberwittler C, Reuther G, Heyen P (1995) Cerebellar herniation in syringomyelia: relation between tonsillar herniation and the dimensions of the syrinx and the remaining spinal cord. A quantitative MRI study. Eur Neurol 35:162–167
McGirt MJ, Nimjee SM, Floyd J, Bulsara KR, George TM (2005) Correlation of cerebrospinal fluid flow dynamics and headache in Chiari I malformation. Neurosurgery 56:716–721
McGirt MJ, Nimjee SM, Fuchs HE, George TM (2006) Relationship of cine phase-contrast magnetic resonance imaging with outcome after decompression for Chiari I malformations. Neurosurgery 59:140–146
McGirt MJ, Atiba A, Attenello FJ, Wasserman BA, Datoo G, Gathinji M, Carson B, Weingart JD, Jallo GI (2008) Correlation of hindbrain CSF flow and outcome after surgical decompression for Chiari I malformation. Childs Nerv Syst 24:833–840
Milhorat TH, Hammock MK, Fenstermacher JD, Rall DP, Levin VA (1971) Cerebrospinal fluid production by the choroids plexus and brain. Science 173:330–332
Milhorat TH, Johnson WD, Miller JI, Bergland RM, Hollenberg-Sher J (1992) Surgical treatment of syringomyelia based on magnetic resonance imaging criteria. Neurosurgery 31:231–245
Milhorat TH, Miller JI, Johnson WD, Adler DE, Heger IM (1993) Anatomical basis of syringomyelia occurring with hindbrain lesions. Neurosurgery 32:748–754
Milhorat TH, Capocelli AL Jr, Anzil AP, Kotzen RM, Milhorat RH (1995) Pathological basis of spinal cord cavitation in syringomyelia: analysis of 105 autopsy cases. J Neurosurg 82:802–812
Milhorat TH, Capocelli AL Jr, Kotzen RM, Bolognese P, Heger IM, Cottrell JE (1997) Intramedullary pressure in syringomyelia: clinical and pathophysiological correlates of syrinx distension. Neurosurgery 41:1102–1110
Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44:1005–1017
Miyasaka K, Asano T, Ushikoshi S, Hida K, Koyanagi I (2000) Vascular anatomy of the spinal cord and classification of spinal arteriovenous malformations. Interv Neuroradiol 6(Suppl 1):195–198
Munshi I, Frim D, Stine-Reyes R, Weir BK, Hekmatpanah J, Brown F (2000) Effects of posterior fossa decompression with and without duraplasty on Chiari malformation-associated hydromyelia. Neurosurgery 46:1384–1390
Muthukumar N, Venkatesh G, Thiruppathy S (2005) Arrested hydrocephalus and the presyrinx state. Case report. J Neurosurg 103(5 Suppl):466–470
Nagib MG (1994) An approach to symptomatic children (ages 4–14 years) with Chiari type I malformation. Pediatr Neurosurg 21:31–35
Nauta HJ, Dolan E, Yasargil MG (1983) Microsurgical anatomy of spinal subarachnoid space. Surg Neurol 19:431–437
Navarro R, Olavarria G, Seshadri R, Gonzales-Portillo G, McLone DG, Tomita T (2004) Surgical results of posterior fossa decompression for patients with Chiari I malformation. Childs Nerv Syst 20:349–356
Netsky MG (1953) Syringomyelia; a clinicopathologic study. AMA Arch Neurol Psychiatry 70:741–777
Nishikawa M, Sakamoto H, Hakuba A, Nakanishi N, Inoue Y (1997) Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 86:40–47
Nomura S, Akimura T, Imoto H, Nishizaki T, Suzuki M (2002) Endoscopic fenestration of posterior fossa arachnoid cyst for the treatment of presyrinx myelopathy–case report. Neurol Med Chir (Tokyo) 42:452–454
Nyland H, Krogness KG (1978) Size of posterior fossa in Chiari type 1 malformation in adults. Acta Neurochir (Wien) 40:233–242
Oldfield EH, Muraszko K, Shawker TH, Patronas NJ (1994) Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg 80:3–15
Olsson B, Eldevik OP, Gronnerod TA (1985) Absorption of iohexol from cerebrospinal fluid to blood: pharmacokinetics in humans. Neuroradiology 27:172–175
Ono A, Suetsuna F, Ueyama K, Yokoyama T, Aburakawa S, Numasawa T, Wada K, Toh S (2007) Surgical outcomes in adult patients with syringomyelia associated with Chiari malformation type I: the relationship between scoliosis and neurological findings. J Neurosurg Spine 6:216–221
Ono A, Suetsuna F, Ueyama K, Yokoyama T, Aburakawa S, Takeuchi K, Numasawa T, Wada K, Toh S (2007) Cervical spinal motion before and after surgery in patients with Chiari malformation type I associated with syringomyelia. J Neurosurg Spine 7:473–477
Padovani R, Cavallo M, Gaist G (1989) Surgical treatment of syringomyelia: favorable results with syringosubarachnoid shunting. Surg Neurol 32:173–180
Panigrahi M, Reddy BP, Reddy AK, Reddy JJ (2004) CSF flow study in Chiari I malformation. Childs Nerv Syst 20:336–340
Perrini P, Benedetto N, Tenenbaum R, Di Lorenzo N (2007) Extra-arachnoidal cranio-cervical decompression for syringomyelia associated with Chiari I malformation in adults: technique assessment. Acta Neurochir (Wien) 149:1015–1023
Phillips TW, Kindt GW (1981) Syringoperitoneal shunt for syringomyelia: a preliminary report. Surg Neurol 16:462–466
Pillay PK, Awad IA, Little JR, Hahn JF (1991) Symptomatic Chiari malformation in adults: a new classification based on magnetic resonance imaging with clinical and prognostic significance. Neurosurgery 28:639–645
Pinna G, Alessandrini F, Alfieri A, Rossi M, Bricolo A (2000) Cerebrospinal fluid flow dynamics study in Chiari I malformation: implications for syrinx formation. Neurosurg Focus 8:E3
Pujol J, Roig C, Capdevila A, Pou A, Marti-Vilalta JL, Kulisevsky J, Escartin A, Zannoli G (1995) Motion of the cerebellar tonsils in Chiari type I malformation studied by cine phase-contrast MRI. Neurology 45:1746–1753
Quigley MF, Iskandar B, Quigley ME, Nicosia M, Haughton V (2004) Cerebrospinal fluid flow in foramen magnum: temporal and spatial patterns at MR imaging in volunteers and in patients with Chiari I malformation. Radiology 232:229–236
Reed CM, Campbell SE, Beall DP, Bui JS, Stefko RM (2005) Atlanto-occipital dislocation with traumatic pseudomeningocele formation and post-traumatic syringomyelia. Spine 30:E128–E133
Rennels ML, Gregory TF, Blaumanis OR, Fujimoto K, Grady PA (1985) Evidence for a 'paravascular' fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:47–63
Resjö IM, Harwood-Nash DC, Fitz CR, Chuang S (1979) Computed tomographic metrizamide myelography in syringohydromyelia. Radiology 131:405–407
Rhoton AL Jr (1976) Microsurgery of Arnold-Chiari malformation in adults with and without hydromyelia. J Neurosurg 45:473–483
Sage MR, Wilcox J, Evill CA, Benness GT (1982) Brain parenchyma penetration by intrathecal ionic and nonionic contrast media. AJNR 3:481–483
Sahuquillo J, Rubio E, Poca MA, Rovira A, Rodriguez-Baeza A, Cervera C (1994) Posterior fossa reconstruction: a surgical technique for the treatment of Chiari I malformation and Chiari I/syringomyelia complex—preliminary results and magnetic resonance imaging quantitative assessment of hindbrain migration. Neurosurgery 35:874–885
Sakamoto H, Nishikawa M, Hakuba A, Yasui T, Kitano S, Nakanishi N, Inoue Y (1999) Expansive suboccipital cranioplasty for the treatment of syringomyelia associated with Chiari malformation. Acta Neurochir (Wien) 141:949–961
Sakas DE, Korfias SI, Wayte SC, Beale DJ, Papapetrou KP, Stranjalis GS, Whittaker KW, Whitwell HL (2005) Chiari malformation: CSF flow dynamics in the craniocervical junction and syrinx. Acta Neurochir (Wien) 147:1223–1233
Sansur CA, Heiss JD, DeVroom HL, Eskioglu E, Ennis R, Oldfield EH (2003) Pathophysiology of headache associated with cough in patients with Chiari I malformation. J Neurosurg 98:453–458
Sato O, Asai T, Amano Y, Hara M, Tsugane R, Yagi M (1971) Formation of cerebrospinal fluid in spinal subarachnoid space. Nature 233:129–130
Schady W, Metcalfe RA, Butler P (1987) The incidence of craniocervical bony anomalies in the adult Chiari malformation. J Neurol Sci 82:193–203
Schlesinger EB, Antunes JL, Michelsen WJ, Louis KM (1981) Hydromyelia: clinical presentation and comparison of modalities of treatment. Neurosurgery 9:356–365
Scholsem M, Scholtes F, Belachew S, Martin D (2008) Acquired tonsillar herniation and syringomyelia after pleural effusion aspiration: case report. Neurosurgery 62:E1172–E1173
Sekula RF Jr, Jannetta PJ, Casey KF, Marchan EM, Sekula LK, McCrady CS (2005) Dimensions of the posterior fossa in patients symptomatic for Chiari I malformation but without cerebellar tonsillar descent. Cerebrospinal Fluid Res 2:11
Sgouros S, Williams B (1995) A critical appraisal of drainage in syringomyelia. J Neurosurg 82:1–10
Sgouros S, Kountouri M, Natarajan K (2007) Skull base growth in children with Chiari malformation Type I. J Neurosurg 107(3 Suppl):188–192
Sindou M, Chavez-Machuca J, Hashish H (2002) Cranio-cervical decompression for Chiari type I-malformation, adding extreme lateral foramen magnum opening and expansile duroplasty with arachnoid preservation. Technique and long-term functional results in 44 consecutive adult cases—comparison with literature dat. Acta Neurochir (Wien) 144:1005–1019
Sivaramakrishnan A, Alperin N, Surapaneni S, Lichtor T (2004) Evaluating the effect of decompression surgery on cerebrospinal fluid flow and intracranial compliance in patients with chiari malformation with magnetic resonance imaging flow studies. Neurosurgery 55:1344–1351
Stevens JM, Serva WA, Kendall BE, Valentine AR, Ponsford JR (1993) Chiari malformation in adults: relation of morphological aspects to clinical features and operative outcome. J Neurol Neurosurg Psychiatry 56:1072–1077
Stoodley MA, Jones NR, Brown CJ (1996) Evidence for rapid fluid flow from the subarachnoid space into the spinal cord central canal in the rat. Brain Res 707:155–164
Stoodley MA, Brown SA, Brown CJ, Jones NR (1997) Arterial pulsation-dependent perivascular cerebrospinal fluid flow into the central canal in the sheep spinal cord. J Neurosurg 86:686–693
Stovner LJ, Rinck P (1992) Syringomyelia in Chiari malformation: relation to extent of cerebellar tissue herniation. Neurosurgery 31:913–917
Stovner LJ, Bergan U, Nilsen G, Sjaastad O (1993) Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:113–118
Tachibana S, Iida H, Yada K (1992) Significance of positive Queckenstedt test in patients with syringomyelia associated with Arnold-Chiari malformations. J Neurosurg 76:67–71
Takayasu M, Takagi T, Hara M, Anzai M (2004) A simple technique for expansive suboccipital cranioplasty following foramen magnum decompression for the treatment of syringomyelia associated with Chiari I malformation. Neurosurg Rev 27:173–177
Tator CH, Meguro K, Rowed DW (1982) Favorable results with syringosubarachnoid shunts for treatment of syringomyelia. J Neurosurg 56:517–523
Tator CH, Briceno C (1988) Treatment of syringomyelia with a syringosubarachnoid shunt. Can J Neurol Sci 15:48–57
Tator CH, Koyanagi I (1997) Vascular mechanisms in the pathophysiology of human spinal cord injury. J Neurosurg 86:483–492
Terae S, Miyasaka K, Abe S, Abe H, Tashiro K (1994) Increased pulsatile movement of the hindbrain in syringomyelia associated with the Chiari malformation: cine-MRI with presaturation bolus tracking. Neuroradiology 36:125–129
Tokuno H, Hakuba A, Suzuki T, Nishimura S (1988) Operative treatment of Chiari malformation with syringomyelia. Acta Neurochir Suppl (Wien) 43:22–25
Trigylidas T, Baronia B, Vassilyadi M, Ventureyra EC (2008) Posterior fossa dimension and volume estimates in pediatri.c patients with Chiari I malformations. Childs Nerv Syst 24:329–336
Tubbs RS, Elton S, Grabb P, Dockery SE, Bartolucci AA, Oakes WJ (2001) Analysis of the posterior fossa in children with the Chiari 0 malformation. Neurosurgery 48:1050–1055
Tubbs RS, McGirt MJ, Oakes WJ (2003) Surgical experience in 130 pediatric patients with Chiari I malformations. J Neurosurg 99:291–296
Tubbs RS, Webb DB, Oakes WJ (2004) Persistent syringomyelia following pediatric Chiari I decompression: radiological and surgical findings. J Neurosurg 100(5 Suppl Pediatrics):460–464
Tubbs RS, Iskandar BJ, Bartolucci AA, Oakes WJ (2004) A critical analysis of the Chiari 1.5 malformation. J Neurosurg 101(2 Suppl):179–183
Ur-Rahman N, Jamjoom ZA (1991) Surgical management of Chiari malformation and syringomyelia: experience in 14 cases. Ann Saudi Med 11:402–410
Vanaclocha V, Saiz-Sapena N, Garcia-Casasola MC (1997) Surgical technique for cranio-cervical decompression in syringomyelia associated with Chiari type I malformation. Acta Neurochir (Wien) 139:529–540
Vaquero J, Mart_nez R, Salazar J, Santos H (1987) Syringosubarachnoid shunt for treatment of syringomyelia. Acta Neurochir (Wien) 84:105–109
Vega A, Quintana F, Berciano J (1990) Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99:137–145
Ventureyra EC, Aziz HA, Vassilyadi M (2003) The role of cine flow MRI in children with Chiari I malformation. Childs Nerv Syst 19:109–113
Vernet O, Farmer JP, Montes JL (1996) Comparison of syringopleural and syringosubarachnoid shunting in the treatment of syringomyelia in children. J Neurosurg 84:624–628
Wang AM, Jolesz F, Rumbaugh CL, Zamani A (1983) CT assessment of thoracic extension and of concomitant lesions in syringohydromyelia. J Comput Assist Tomogr 7:18–24
Wetjen NM, Heiss JD, Oldfield EH (2008) Time course of syringomyelia resolution following decompression of Chiari malformation Type I. J Neurosurg Pediatr 1:118–123
Williams B (1969) The distending force in the producing of “communicating syringomyelia”. Lancet 26:189–193
Williams B (1980) On the pathogenesis of syringomyelia: a review. J R Soc Med 73:798–806
Williams B, Sgouros S, Nenji E (1995) Cerebrospinal fluid drainage for syringomyelia. Eur J Pediatr Surg 5(Suppl 1):27–30
Winkler SS, Sackett JF (1980) Explanation of metrizamide brain penetration: a review. J Comput Assist Tomogr 4:191–193
Wolpert SM, Bhadelia RA, Bogdan AR, Cohen AR (1994) Chiari I malformations: assessment with phase-contrast velocity MR. AJNR 15:1299–1308
Won DJ, Nambiar U, Muszynski CA, Epstein FJ (1997) Coagulation of herniated cerebellar tonsils for cerebrospinal fluid pathway restoration. Pediatr Neurosurg 27:272–275
Woosley RE, Whaley RA (1982) Use of metrizamide in computerized tomography to diagnose the Chiari I malformation. J Neurosurg 56:373–376
Wu YW, Chin CT, Chan KM, Barkovich AJ, Ferriero DM (1999) Pediatric Chiari I malformations: do clinical and radiologic features correlate? Neurology 53:1271–1276
Yamazaki Y, Tachibana S, Takano M, Fujii K (1998) Clinical and neuroimaging features of Chiari type I malformations with and without associated syringomyelia. Neurol Med Chir (Tokyo) 38:541–546
Yeh DD, Koch B, Crone KR (2006) Intraoperative ultrasonography used to determine the extent of surgery necessary during posterior fossa decompression in children with Chiari malformation type I. J Neurosurg 105(1 Suppl):26–32
Yilmaz N, Kiymaz N, Mumcu C (2005) Surgical treatment of craniocervical decompression without Chiari malformation in syringomyelia. Hiroshima J Med Sci 54:109–111
Yundt KD, Park TS, Tantuwaya VS, Kaufman BA (1996) Posterior fossa decompression without duraplasty in infants and young children for treatment of Chiari malformation and achondroplasia. Pediatr Neurosurg 25:221–226
Author information
Authors and Affiliations
Corresponding author
Additional information
Comments
Fumio Suzuki and Kazuhiko Nozaki, Shiga, Japan
The authors are to be congratulated for this comprehensive overview on the pathophysiology of syringomyelia. They made a modification of the theory proposed by Greitz D. in that a decreased compliance of the large veins in the subarachnoid space, which results from the reduced compliance of CSF below the obstruction, decreases the absorption of the extracellular fluid from intramedullary venous channels, resulting in the accumulation of extracellular fluid in spinal cord. This phenomenon might contribute partly to the development of syringomyelia but does not seem to be a main cause of syrinx formation. Although Greitz D. reported in his review that venous congestion might contribute to syrinx formation, venous congestion is not so obvious in Chari malformation type 1 as in spinal dural AVFs, in which large veins of the spinal cord are congested severely and compromised veins should reduce their compliance. These abnormal venous conditions may induce necrotizing myelitis but do not necessarily accompany syrinx formation. The authors referred to the report by Heiss J. et al. as an evidence of reduced CSF compliance, but the data was not statistically significant. More data about the changes in compliance of CSF space in Chiari Type 1 should be needed before establishing their modified theory.
Comments
Ricardo V. Botelho, São Paulo, Brazil
The authors performed a comprehensive review of mechanisms and concepts related to the pathogenesis of syringomyelia in Chiari malformation and have designed a hypothetical model of pathogenesis for syringomyelia.
Some of the factors reviewed are well established and others are hypothetical:
1. Patients with CM and sirirngomielia have smaller posterior fossa than those who did not have syringomyelia.
2. In patients with Chiari malformation, smaller tonsillar herniations are associated more frequently with syringomyelia than larger herniations.
The combination of these two features, small and shallow posterior fossa and small herniation of the tonsils might suggest a lower compliance of the foramen magnum, at the same time, prevents the descent of the tonsils and produces an early and intense blockage of free flow of craniocervial CSF in patients with syrinx.
3. Patients with syringomyelia have a blockage of subarachnoid CSF flow and less complacency of the subarachnoid space and posterior spinal veins.
4. The reduced absortion mechanism from the extracellular fluid from the spinal Cord parenchyma would result in syringomyelia in Chiari type 1 malformation, as speculated by the authors.
One real and observed effect in patients with syringomyelia and MC is that decompression of the posterior fossa often decreases syringomyelia cavity, probably by restoring the caniocervical flow of CSF.
The importance of reducing capacity venos absorption of extracellular fluid is an interesting suggestion posed by the authors that future works will confirm or not these suggestions.
Comments
Jörg Klekamp, Quakenbrück, Germany
In this paper, Koyanagi and Houkin present a hypothesis that was supposed to explain the development of syringomyelia in patients with a Chiari type I malformation. The authors correctly summarize in their paper that previous theories trying to explain syringomyelia by cerebrospinal fluid (CSF) entering the spinal cord via the 4th ventricle or other avenues have failed to demonstrate such a communication and are not able to explain several observations in these patients. Even though several thoughts and conclusions by the authors are well founded, I do have some reservations against this paper.
In table 1, the authors provide a list of previous theories and disqualify each of these as speculative. This statement is grossly negligent. Gardner's and Williams' theories, for instance, may no longer be tenable but were based on careful clinical tests, pressure recordings in patients and several animal studies. Given the technical conditions at the time, these works were state of the art and well founded on the observations made. Likewise, the theories of extracellular origin relating syringomyelia to edema formation are based on animal experiments and clinical observations and by no means just the result of a literature review.
The concept of syringomyelia as a spinal cord edema is by no means new. Tannenberg in 1924 and Liber and Lisa in 1937 were the first to propose this view. Taylor and Byrnes in 1974, Aboulker in 1979, and Yamada et al. in 1996 further elaborated on this theory and already emphasized the importance of venous obstruction, which they thought to cause syrinx formation in combination with CSF flow obstruction.
I do not agree with the authors' initial statement, that theories concerning the pathophysiology of syringomyelia on this basis do not apply to patients with a Chiari malformation. Several experimental studies have provided new insights into the physiological exchange between extracellular fluid (ECF) of the spinal cord and CSF under normal conditions as well as with CSF-flow obstructions. It appears that any pathology causing a CSF-flow obstruction and/or spinal cord tethering as well as certain intramedullary tumors are able to disturb the balance between ECF und CSF in the spinal canal, which may then lead to syrinx formation. This concept applies to patients with a Chiari malformation just as well as to those with posttraumatic syringomyelia, for instance. After all, syrinx formation in Chiari patients is the result of CSF-flow obstruction at the foramen magnum as it is in posttraumatic syringomyelia with CSF-flow obstruction at the level of the posttraumatic arachnopathy. With their hypothesis, Koyanagi and Houkin simply add a reduced compliance of posterior spinal cord veins to this concept of ECF/CSF imbalance. Spinal cord veins may turn out to contribute to syrinx formation in this setting but this assumption does not imply a completely novel hypothesis.
References
1. Aboulker J. (1979) La syringomyelie et les liquides intra-rachidiens. Neurochirurgie 25 (Suppl):1–144.
2. Liber AF, Lisa JR. (1937) Rosenthal fibres in non-neoplastic syringomyelia: a note on the pathogenesis of syringomyelia. J. Nerv. Ment. Dis. 86:549–558.
3. Tannenberg J. (1924) Über die Pathogenese der Syringomyelie, zugleich ein Beitrag zum Vorkommen von Capillarhämangiomen im Rückenmark. Z. Neurol. 92:119–174.
4. Taylor AR, Byrnes DP. (1974) Foramen magnum and high cervical cord compression. Brain 97:473–480.
5. Yamada H, Yokota A, Haratake J, Horie A. (1996) Morphological study of experimental syringomyelia with kaolin-induced hydrocephalus in a canine model. J. Neurosurg. 84:999–1005.
Rights and permissions
About this article
Cite this article
Koyanagi, I., Houkin, K. Pathogenesis of syringomyelia associated with Chiari type 1 malformation: review of evidences and proposal of a new hypothesis. Neurosurg Rev 33, 271–285 (2010). https://doi.org/10.1007/s10143-010-0266-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10143-010-0266-5