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Classification of syringomyelia

THOMAS H. MILHORAT, M.D. Department of , State University of New York, Health Science Center at Brooklyn, and the Kings County Hospital Center, Brooklyn, New York

Syringomyelia poses special challenges for the clinician because of its complex symptomatology, uncertain patho- genesis, and multiple options of treatment. The purpose of this study was to classify intramedullary cavities according to their most salient pathological and clinical features. Pathological findings obtained in 175 individuals with tubular cavitations of the were correlated with clinical and magnetic resonance (MR) imaging findings in a database of 927 patients. A classification system was developed in which the morbid anatomy, cause, and pathogenesis of these lesions are emphasized. The use of a disease-based classification of syringomyelia facilitates diagnosis and the interpretation of MR imag- ing findings and provides a guide to treatment.

KEY WORDS • • • • posttraumatic syringomyelia • • tethered spinal cord

Previous attempts to classify syringomyelia have been spinal cord. There were 94 males and 81 females who had based on presumed mechanisms of pathogenesis.1–3,5,6,20 ranged in age from 1 day to 87 years (mean age 41.6 These classifications have been useful and have helped to years). In all cases a standard complete autopsy was per- shape surgical treatment. However, with the advent of MR formed. After opening the cranial cavity, the upper end of imaging it has become evident that some concepts of the spinal cord was divided at the foramen magnum and pathogenesis are no longer tenable. Chief among these is removed with the brain side of the specimen. The remain- the hypothesis that syrinx formation depends on the force- der of the spinal cord was removed via the abdominal and ful diversion of CSF from the fourth ventricle into the cen- thoracic cavities, as described elsewhere.10 The review of tral canal of the spinal cord.7,19,20 histological material was facilitated by an institutional Contributing to the difficulty of defining mechanisms policy that requires that original slides and paraffin blocks of syrinx formation has been the general lack of infor- be retained with the permanent autopsy file. Old and new mation on pathological features. Although Netsky15 has paraffin blocks were cut serially to a thickness of 6 µ reported on eight autopsy cases, with few exceptions most mounted on glass slides, and stained with hematoxylin studies prior to 1990 were case reports. In recent years, and eosin. Supplemental stains included Luxol fast blue, reports have appeared that help to clarify the pathological Weil stain, Gomori's stain, Bodian's stain, periodic-acid features of spinal cord cavitation.8,10 These data, taken to- Schiff, phosphotungstic acid hematoxylin, and glial fibril- gether with MR imaging correlates, permit a reclassifica- lary acidic protein. Histological sections were viewed tion of syringomyelia based on morbid anatomy. through a microscope at magnifications ranging from 10 to 1000. Final diagnoses were as follows: nonneo- CLINICAL MATERIAL AND METHODS plastic syringomyelia in 105 cases; syringomyelia ex vacuo in 52 cases; and neoplastic in 18 cases. The Autopsy Data pathological findings in 105 cases of nonneoplastic syrin- gomyelia have been previously published.10 Between the years 1955 and 1993 autopsies were per- formed in 175 cadavers with tubular cavitations of the Clinical Data Nine hundred twenty-seven patients with cavitary le- Abbreviations used in this paper: CCS = stenosis; sions of the spinal cord were evaluated between the years CSF = ; MR = magnetic resonance. 1990 and 1998. There were 382 male and 545 female

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Fig. 2. Magnetic resonance imaging studies demonstrating communicating syringomyelia of the cervical spine in a 58-year- old male with posthemorrhagic hydrocephalus and syringomyelia. Left: Sagittal image demonstrating that the syrinx is continuous with the fourth ventricle. Right: Axial image revealing a symmet- rically enlarged central cavity.

Fig. 1. Diagrammatic and photomicrographic depictions of the CSF pathways distal to the outlets of the fourth ventri- communicating syringomyelia. Left: Diagram illustrating the cle (Fig. 1). In typical cases, there is generalized enlarge- pathological findings obtained in a 49-year-old male with post- ment of all four cerebral ventricles, and the central canal meningitic hydrocephalus, basilar arachnoiditis, and syringomye- participates in the hydrocephalic process like a "fifth ven- lia. The syrinx is anatomically continuous with the enlarged fourth ventricle (4th) and its length has been determined by CCS. tricle." Causative factors include postmeningitic and Right: Photomicrographs of specimens obtained in the same posthemorrhagic hydrocephalus, complex hindbrain mal- patient. H & E. A: Axial section obtained through the syrinx at formations, such as Chiari II malformation and enceph- T-1, showing a central cavity lined by . Original magni- alocele, and Dandy–Walker cysts. An experimental model fication 10. B: Axial section obtained immediately below the of communicating syringomyelia can be produced by in- syrinx at T-10, demonstrating occlusion of the central canal jecting kaolin into the cisterna magna.4,21 (arrow). Original magnification 40. On histological examination, communicating syringes appear as simple dilations of the central canal, lined whol- ly or partially by ependyma (Fig. 1A). In acquired exam- patients who ranged in age from 8 months to 82 years ples, the length of the cavity is defined caudally by central (mean age 38.2 years). Each patient underwent a detailed canal stenosis (Fig. 1B), which is an age-related phenom- neurological examination and at least one MR imaging enon affecting the majority of normal individuals by the session of the spinal cord that included the area of cavita- early years of adult life.13 Holocord enlargements are most tion and the cervicomedullary junction. In many cases, often of congenital origin and may be anatomically con- additional information was provided by the whole-brain tinuous with caudal lesions such as myelomeningocele. and spinal cord MR images, cine MR imaging, computer- With distension of the central canal, the ependymal epi- ized tomography , somatosensory evoked thelium becomes stretched and denuded. Nevertheless, potentials, and other neurodiagnostic tests. The protocol despite the large size of some communicating syringes, for diagnostic workup and the specific techniques of neu- these lesions are much less prone than noncommunicating roimaging have been previously published.11 syringes to rupture paracentrally, and this may explain why a significant number of communicating syringes re- main asymptomatic throughout life or are associated with RESULTS only minor neurological findings.10,12 Figure 2 illustrates Tubular enlargements of the spinal cord that are not due the MR imaging correlates of communicating syringo- to intramedullary tumors have been classified as follows myelia. on the basis of pathological findings:10 1) dilations of the central canal that are anatomically continuous with the Noncommunicating Central Canal Dilations fourth ventricle (communicating syringomyelia); 2) dila- Dilations of the central canal that do not communciate tions of the central canal that do not communicate with the with the fourth ventricle are associated with obstructions fourth ventricle (noncommunicating syringomyelia); and of the CSF pathways at or below the foramen magnum. 3) extracanalicular syringes that originate in the spinal Causative factors include the Chiari I malformation, bas- cord parenchyma and do not communciate with the cen- ilar invagination, spinal arachnoiditis, extramedullary tral canal or fourth ventricle (primary parenchymal cavi- compressions, tethered cord, and acquired tonsillar herni- tations). These lesions are distinguished from two other ation. There is accumulating evidence that the formation types of cavitation: 1) atrophic syringes occurring with of noncommuniating syringes depends on an increase of myelomalacia (syringomyelia ex vacuo); and 2) neoplas- 12 the arterial pulse wave in the spinal subarachnoid space tic cysts. that is sufficient to force CSF through anatomically con- tinuous perivascular and interstitial spaces into the central Communicating Central Canal Dilations canal of the spinal cord.14,16–18 An experimental model of Communicating syringes are caused by obstructions of noncommunicating syringomyelia can be produced by

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Fig. 4. Diagrammatic and photomicrographic depictions of noncommunicating central canal dilation. Left: Diagram illustrat- Fig. 3. Diagrammatic and photomicrographic representations of ing the pathological findings obtained in a 62-year-old female with noncommunicating central canal dilation. Left: Diagram illustrat- a Chiari I malformation and syringomyelia. The syrinx is defined ing the pathological findings obtained in a 66-year-old male with rostrally and caudally by CCS. At C-7, the syrinx has ruptured into syringomyelia occurring in association with basilar invagination the dorsal columns and dissected rostrally above the and a Klippel–Feil anomaly. The syrinx is defined rostrally and original cavitation. Clinical findings while the patient was alive caudally by CCS and was asymptomatic during life. Right: Pho- included numbness and clawing of the left hand, impaired position tomicrographs of specimens obtained in the same patient. H & E, sense, and spastic weakness of the legs. Right: Photomicrographs original magnification 40. A: Axial section immediately rostral of specimens obtained in the same patient. H &E, original magni- to the syrinx showing occlusion of the central canal (arrow). B: fication 40. A: Axial sections of the spinal cord obtained at Axial section obtained through the syrinx at T-3, demonstrating C-4, showing an extracanalicular cavitation of the dorsal white dilation of the central canal with some denuding of the ependyma. matter columns. The central canal is stenotic (arrow). B: Axial section through the syrinx obtained at C-7, demonstrating an ependymal-lined cavity that has ruptured through the dorsal root entry zone on the left to communicate with the subarachnoid space. injecting kaolin into the central canal and regional me- ninges.14,18 On histological examination, noncommunicating sy- fluid from the subarachnoid space into the interstitial ringes appear as isolated cavities that are defined rostrally spaces of the spinal cord.4,10 and caudally by central spinal canal stenosis (Fig. 3). Primary parenchymal cavitations typically arise in the These cavities tend to be complex lesions and are charac- watershed area of the spinal cord, dorsal and lateral to the terized histologically by extensive areas of ependymal central canal. Like the paracentral dissections of central denuding, paracentral dissection, and the formation of in- tracanalicular septae.10 In contrast to communicating sy- ringes, which rarely rupture paracentrally, noncommuni- cating syringes exhibit a propensity for dissecting into the spinal cord parenchyma (Fig. 4). Parenchymal dissections occur preferentially into the dorsolateral quadrant of the spinal cord and may extend through the pial surface to communicate with the subarachnoid space. Neurological findings can often be correlated with the anatomy of cav- itation demonstrated on MR imaging (Figs. 5 and 6). Primary Parenchymal Cavitations These lesions consist of tubular cavitations of the spinal cord that originate in the parenchyma and do not commu- nicate with the central spinal canal or fourth ventricle (Fig. 7). A distinguishing feature of this type of syringomyelia is its association with conditions that injure the spinal cord Fig. 5. Magnetic resonance images demonstrating noncommu- tissue. Common causative factors include trauma, isch- nicating central canal dilation of the cervical spine in a 42-year-old female with a Chiari I malformation and syringomyelia. Clinical emia/infarction, and spontaneous intramedullary hemor- findings were limited to fatigue and weakness of the extremities rhage. Although the mechanism by which parenchymal and hyperreflexia. Left: Sagittal image revealing that the syrinx is cavities fill and distend is incompletely understood, cur- separated from the fourth ventricle by a long, syrinx-free segment rent evidence suggests that arachnoiditis occurring at the of spinal cord. Right: Axial image obtained through syrinx at time of produces a regional CSF block that forces T-1, demonstrating a symmetrically enlarged central cavity.

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Fig. 7. Diagrammatic and photomicrographic representations of primary parenchymal cavitation. Left: Diagram of pathological findings obtained in a 62-year-old female with posttraumatic syrin- gomyelia who had been paraplegic for 23 years following a motor vehicle accident. The syrinx occupies three quadrants of the spinal Fig. 6. Magnetic resonance images demonstrating noncommu- cord and does not communicate with the central canal. Right: nicating central canal dilation of the cervical spine in a 24-year-old Photomicrographs of sections obtained in the same patient. H & E. female with a Chiari I malformation and syringomyelia. Neuro- A: Axial sections obtained through the syrinx at T-2, showing a large, irregular parenchymal cavity. The central canal is occluded logical findings included a decreased left-sided corneal reflex, im- paired pain and temperature sensation involving all three divisions (arrow). Original magnification 10. B: Axial section obtained of the left , weakness of the left arm and leg, through the injury site at T-8, demonstrating a glial scar with hemo- siderin-laden macrophages (larger arrow) and a stenotic central patchy analgesia of the left arm, and impaired pain and temperature sensation below T-2 on the right. Upper Left: Sagittal image canal (smaller arrow). Original magnification 40. revealing a noncommuniating syrinx (C-1 to T-2) and a Chiari I malformation. Upper Right: Axial image obtained through syr- inx at C-5, demonstrating a symmetrically enlarged central cavity. , and other less common . The Lower Left and Right: Axial images obtained above C-4 demon- necrotic process begins centrally and tends to extend ros- strating that the syrinx has expanded into the left dorsolateral quad- rant of the spinal cord (lower left) and dissected rostrally to enter trally or caudally from the poles of the tumor. Neoplastic the medulla on the left side (lower right). cysts contain proteinaceous fluid that is quite different from CSF, and the walls of the are lined by tumor or tightly packed glial tissue around a mural nodule. The di- canal syringes, these lesions are lined by glia or fibroglial agnosis is established by performing contrast-enhanced tissue, and they are characterized histologically by vary- MR imaging (Fig. 10). ing degrees of necrosis, neuronophagia, and wallerian de- 10 generation. A particularly common histological finding DISCUSSION is the presence of hemosiderin-laden macrophages in the walls of cavities caused by trauma or hemorrhage. Figure Table 1 provides a classification of syringomyelia based 8 illustrates the MR imaging correlates of this type of syr- on pathological findings and MR imaging correlates. The ingomyelia. separation of syringes into communicating, noncommuni- cating, and atrophic types implies mechanisms of patho- Atrophic Cavitations (Syringomyelia Ex Vacuo) genesis. Causative factors have been summarized accord- Degenerative changes occurring in conjunction with ing to standard nomenclature. The inclusion of neoplastic spinal cord atrophy can lead to the formation of micro- cavitations in this classification system is meant to em- cysts, intramedullary clefts, and localized dilations of the phasize their importance in the differential diagnosis of central spinal canal. Atrophic cavitations do not propa- syringomyelia rather than to suggest any pathological gate, presumably because of the absence of a filling mech- similarities. anism, and are caused by the loss of parenchymal tissue The use of a disease-based classification of syringo- (syringomyelia ex vacuo). On MR imaging, these lesions myelia facilitates diagnosis and the interpretation of MR appear as nondistended cavities confined to the area of imaging findings. With this system, it is possible in myelomalacia (Fig. 9). most cases to establish clinicopathological correlations (see Figs. 3–8). The ability of MR imaging to distinguish Neoplastic Cavitations between communicating, noncommunicating, and atroph- Syrinx-like cavities can be formed by the cystic degen- ic syringes has treatment implications. For example, com- eration of intramedullary tumors such as astrocytomas, municating syringes are generally treated by placing ven-

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Fig. 10. Magnetic resonance images demonstrating a neoplastic cyst of the cervical spine in a 21-year-old female with a cystic intramedullary . The tumor is difficult to see on a noncontrast-enhanced image (left) but enhances brilliantly after the adminsitration of gadolineum (right).

a disease-based system provides a solid foundation for di- agnosis and treatment.

Acknowledgments The following individuals helped to prepare the manuscript and Fig. 8. Magnetic resonance images demonstrating primary par- photographic materials for electronic publishing: Pierre S. Girgis, enchymal cavitation of the cervical spine in a 43-year-old female M.D., Robert H. Milhorat, M.B.A., John T. Milhorat, and Jill Gret- with posttraumatic syringomyelia and burning dysesthesias of the enstein. left arm and upper chest. Neurological findings included weakness of the left arm and leg, areflexia of the left arm, and impaired sen- References sation with trophic changes from C-5 to T-4 on the left side. Upper Left: Sagittal image revealing congenital stenosis of the cer- 1. Barnett HJM: Syringomyelia associated with spinal arachnoidi- vical spine and noncommunicating syringomyelia (C-4 to C-7). tis, in Barnett HJM, Foster JB, Hudgson P (eds): Syringomy- Upper Right: Horizontal image demonstrating lateralization of the elia. London: WB Saunders, 1973, pp 220–244 syrinx to the left hemicord. Lower Left: Axial image obtained at 2. Barnett HJM, Jousse AT, Ball MJ: Pathology and pathogenesis C-5 demonstrating that the syrinx occupies the left dorsolateral of progressive cystic as a late sequel to spinal cord quadrant of the spinal cord. injury, in Barnett HJM, Foster JB, Hudgson P (eds): Syringo- myelia. London: WB Saunders, 1973, pp 179–219 3. Batzdorf U: Classification of syringomyelia, in Batzdorf U (ed): Syringomyelia. Current Concepts in Diagnosis and Treat- tricular shunts. In the case of noncommunicating syringes, ment. Baltimore: Williams & Wilkins, 1991, pp 1–2 the goal of is to relieve the CSF obstruction, and shunt placement is reserved as a secondary procedure.9,11 Atrophic syringes are obviously not treated surgically. Overall, although no classification is truly ideal, the use of TABLE I Classification of syringomyelia

I communicating syringomyelia central canal dilations 1) communicating hydrocephalus (posthemorrhagic, postmeningitic) 2) complex hindbrain malformations (Chiari II, ) 3) Dandy–Walker cyst II noncommunicating syringomyelia central canal/paracentral syringes 1) Chiari malformations 2) basilar invagination 3) spinal arachnoiditis (posttraumatic, postmeningitic) 4) extramedullary compressions (spondylosis, tumors, cysts) 5) tethered cord 6) acquired tonsillar herniation (hydrocephalus, intracranial Fig. 9. Magnetic resonance images demonstrating syringo- mass lesions, craniosynostosis) myelia ex vacuo of the cervical spine in a 76-year-old male with primary parenchymal cavitations progressive myelopathy. Left: Sagittal image revealing cervical 1) spinal cord trauma spondylosis and a small intramedullary cleft within an area of my- 2) ischemia/infarction elomalacia (arrow). Right: Axial image revealing a transversely 3) intramedullary hemorrhage collapsed cavity (arrow) that extends into the dorsal columns of the III atrophic cavitations (syringomyelia ex vacuo) spinal cord. IV neoplastic cavitations

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4. Eisenberg HM, McLennan JE, Welch K: Ventricular perfusion Experimental model and histological findings. J Neurosurg in cats with kaolin-induced hydrocephalus. J Neurosurg 41: 78:274–279, 1993 20–28, 1974 15. Netsky MG: Syringomyelia: a clinicopathologic study. Arch 5. Finlayson AI: Syringomyelia and related conditions, in Baker Neurol Psychiatry 70:741–777, 1953 AB (ed): Clinical Neurology. New York: Harper & Row, 16. Oldfield EH, Muraszko K, Shawker TH, et al: Pathophysiology 1978, pp 1–14 of syringomyelia associated with Chiari I malformation of the 6. Gardner WJ, Angel I: The cause of syringomyelia and its surgi- cerebellar tonsils. Implications for diagnosis and treatment. J cal treatment. Cleve Clin Q 25:4–8, 1958 Neurosurg 80:3–15, 1994 7. Gardner WJ, Goodall RJ: The surgical treatment of Arnold- 17. Stoodley MA, Brown SA, Brown CJ, et al: Arterial pulsation- Chiari malformation in adults. An explanation of its mechanism dependent perivascular cerebrospinal fluid flow into the central and importance of encephalography in diagnosis. J Neurosurg canal in the sheep spinal cord. J Neurosurg 86:686–693, 1997 7:199–206, 1950 18. Stoodley MA, Gutschmidt B, Jones NR: Cerebrospinal fluid 8. Hinokuma K, Ohama E, Oyanagi K, et al: Syringomyelia. A flow in an animal model of noncommunicating syringomyelia. neuropathological study of 18 autopsy cases. Acta Pathol Jpn Neurosurgery 44:1065–1076, 1999 42:25–34, 1992 19. Williams B: The distending force in the production of "commu- 9. Klekamp J, Batzdorf U, Samii M, et al: Treatment of syringo- nicating syringomyelia." Lancet 2:189–193, 1969 myelia associated with arachnoid scarring caused by arach- 20. Williams B: On the pathogenesis of syringomyelia: a review. J noiditis or trauma. J Neurosurg 86:233–240,1997 R Soc Med 73:798–806, 1980 10. Milhorat TH, Capocelli AL Jr, Anzil AP, et al: Pathological 21. Williams B, Bentley J: Experimental communicating syringo- basis of spinal cord cavitation in syringomyelia: analysis of 105 myelia in dogs after cisternal kaolin injection. Part 1. Morphol- autopsy cases. J Neurosurg 82:802–812, 1995 ogy. J Neurol Sci 48:93–107, 1980 11. Milhorat TH, Johnson RW, Milhorat RH, et al: Clinicopatho- logical correlations in syringomyelia using axial magnetic res- onance imaging. Neurosurgery 37:206–213, 1995 12. Milhorat TH, Johnson WD, Miller JI, et al: Surgical treatment Manuscript received January 7, 2000. of syringomyelia based on magnetic resonance imaging crite- Accepted in final form January 31, 2000. ria. Neurosurgery 31:231–245, 1992 Address reprint requests to: Thomas H. Milhorat, M.D., Box 13. Milhorat TH, Kotzen RM, Anzil AP: Stenosis of central canal 1189, 450 Clarkson Avenue, State University of New York, Health of spinal cord in man: incidence and pathological findings in Science Center at Brooklyn, Brooklyn, New York 11203 232 autopsy cases. J Neurosurg 80:716–722, 1994 Figures 1, 3, 4, and 7 were published in part or in whole in the 14. Milhorat TH, Nobandegani F, Miller JI, et al: Noncommunica- Journal of Neurosurgery. Figures 2, 6, 8, 9, and 10 are reprinted ting syringomyelia following occlusion of central canal in rats. with permission from Neurosurgery.

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