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.
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Introduction
The exact pathogenesis of syringomyelia associated with Chiari type 1 malformation has not been clarified. This disorder is characterized by ectopia of the cerebellar tonsils with or without displacement of the brainstem through the foramen magnum. Disturbed pathway of the cerebrospinal fluid (CSF) around the foramen magnum is assumed to be the primary cause of syringomyelia. However, hydrocephalus is usually absent, and the degrees of subarachnoid blockade at the foramen magnum and descent of the cerebellar tonsils are not associated with presence or absence of syringomyelia. Although recent advances of neuroradiological imaging provided static and dynamic information on the anatomical structures around the foramen magnum, none of the previously reported theories fully explained the clinical or radiological features. Until now, no animal models successfully reproduced this disorder. In the known experimental models, syringomyelia was produced by induction of adhesive arachnoiditis, spinal cord injury or hydrocephalus.
In this article, we critically review the previously proposed theories and clinical studies of syringomyelia associated with Chiari type 1 malformation. The anatomical and pathophysiological evidences are analyzed to infer the mechanisms of syrinx formation. The purpose of this review is to create a new hypothesis for the pathogenesis of syringomyelia associated with Chiari type 1 malformation.
Previous theories for the pathogenesis
Table 1 summarizes the previously reported theories. Most of theories in 1900s focused on how CSF entered into the spinal cord as the pathogenesis of syringomyelia [16, 57–59, 130, 145, 200, 201]. The main source of CSF entrance was considered to be the fourth ventricle via the central canal [57–59, 200, 201] or the spinal subarachnoid space via the perivascular spaces [16, 130, 145]. The latter theory that the syrinx fluid originates from the subarachnoid CSF has been supported by many clinical or experimental studies. However, the subarachnoid CSF origin theory was not based on direct evidences. Recent articles in 2000s proposed that the syrinx fluid derived from the extracellular fluid from the spinal cord microcirculation, not from the CSF in the subarachnoid space or the fourth ventricles [69, 70, 104, 115]. These studies did not show new clinical evidences but provided novel insights into the pathogenesis of syringomyelia. The idea that the syrinx fluid originates from the extracellular fluid may explain the pathophysiology of syrinx formation in adhesive spinal arachnoiditis but is still difficult to explain effectively the mechanism in Chiari type 1 malformation.
Clinicopathological studies
There have been only several studies reporting human spinal cord specimens of syringomyelia with Chiari type 1 malformation. In 1953, Netsky reported autopsy findings of 8 patients with syringomyelia and found abnormal vessels around the syringes [141]. He suggested that the intramedullary abnormal vessels were the cause of syringomyelia. However, Chiari malformation was present in only one patient in the series. From 1987 to 1996, autopsy findings of 18 cases of syringomyelia with Chiari type 1 malformation were reported in four papers [20, 80, 91, 132]. These studies demonstrated that there was no direct communication between the fourth ventricle and the syrinx, but the central canal to the fourth ventricle was patent in eight of these 18 cases. Ependymal lining of the syrinx or communication of the syrinx with the central canal was observed in all cases. The syrinx usually extended into the posterior gray matter and sometimes communicated with the spinal subarachnoid space.
Radiological evidences of CSF dynamics
CT-scan with intrathecal water-soluble contrast materials
Computed tomographic (CT) scan after intrathecal administration of water-soluble contrast materials (CT myelography (CTM)) was introduced for radiological examination of syringomyelia in the end of 1970s [51, 159]. The delayed CTM several hours after intrathecal injection of metrizamide (MW 789) displayed enhancement of syringomyeliac cavities [13, 26, 27, 29, 35, 100, 101, 111, 117, 168, 198, 206]. Such CTM findings supported the theory of parenchymal CSF entrance because the contrast medium injected into the spinal subarachnoid space was accumulated in the syrinx without entrance into the fourth ventricle. Similar intramedullary contrast accumulation was also present in other intramedullary cystic lesions in cervical spondylosis, intramedullary tumors, and syringomyelia due to other etiologies [95, 99].
Several studies demonstrated dynamics of the intrathecally injected water-soluble contrast materials in the normal spinal cord. These studies indicated that a significant part of the intrathecally injected metrizamide was eliminated to the blood via the spinal routes in rabbits [66] and humans [45, 146]. It is also known that the intrathecally injected water-soluble contrast materials penetrate into the normal brain and spinal cord parenchyma in dogs [40, 161], rabbits [44, 85] and humans [86, 88, 203]. The mechanism of metrizamide penetration from the subarachnoid space into the spinal cord was thought to be a simple diffusion because of lack of a barrier between subarachnoid CSF and the extracellular fluid of the spinal cord. Tracer studies using HRP (MW 43,000) demonstrated rapid entrance of the subarachnoid HRP into the spinal cord [176, 177] or the brain [179] via the perivascular spaces in normal rats, cats, dogs and sheep. These studies suggested the role of arterial pulsation as a driving force.
Considering the results of CTM and tracer studies, intramedullary penetration of the water-soluble contrast materials from the subarachnoid space will not be specific to syringomyelia. Delayed clearance of the contrast from the syrinx cavities may explain delayed visualization of the syrinx in CTM.
CSF dynamics by cine-mode MR imaging
Cine-mode magnetic resonance (MR) imaging enables analysis of CSF dynamics in a cardiac cycle in the patients with Chiari type 1 malformation. Most of the published studies utilized phase-contrast techniques [3, 6, 21, 28, 38, 69, 74, 76, 83, 90, 105, 120, 126–128, 150, 154–156, 174, 196, 204]. Some studies demonstrated CSF movement as the displacement of the bands [185] or stripes [164]. According to these MR studies, there was a significant variety in the degree of subarachnoid blockade and physiological parameters of the CSF flow in Chiari type 1 malformation. The CSF movement in the posterior subarachnoid space at the foramen magnum was disturbed or completely blocked by the displaced cerebellar tonsils. However, some studies on pediatric population reported normal CSF flow in 19–33% of the patients with Chiari type 1 malformation [126, 127, 196]. The reported data on the CSF velocities in the spinal subarachnoid space were more confusing. Some studies [3, 6, 21, 164] reported that the systolic CSF velocities in Chiari patients were lower than those in healthy controls. Other studies [76, 89, 120] reported significantly higher systolic velocities. Simultaneous bidirectional CSF flow at the foramen magnum was also reported [190]. None of cine-mode MR imaging studies showed CSF entrance from the fourth ventricle or the spinal subarachnoid space into the syrinx. Also, most of them did not explain why some Chiari patients developed syringomyelia and others did not. Only one study compared cine MR findings of 32 patients with syringomyelia and 15 patients without syringomyelia in Chiari type 1 malformation [154] and reported that the duration of the caudal CSF movement in the ventral subarachnoid space was significantly longer in syringomyelia.
Thus, the cine-mode MR imaging studies demonstrated abnormal CSF dynamics in Chiari type 1 malformation. However, they failed to display definite evidences that CSF enters into the syrinx.
Pressure studies of syringomyelia
Direct recordings of the pressure in the syrinx were performed in four studies [34, 46, 76, 133]. In 1970, Ellertsson and Greitz first recorded pressures of the subarachnoid space and the syrinx using electromanometric equipment after percutaneous puncture in ten patients [46]. They described that the pressures in the syrinx were above those in the subarachnoid space in most cases, but the difference was not significant. Unfortunately, they did not specify the type of syringomyelia. Davis and Symon recorded the intrasyrinx pressure with a simple manometric technique during surgery in 17 syringomyelic patients including 5 Chiari malformations [34]. The recorded pressures were relatively low (4.0 to 7.0 cmH2O in 15 patients and 0 to 1.0 cmH2O in the other two patients) probably because their measurement was performed after draining of the subarachnoid CSF and syringomyelic fluid. Milhorat et al. performed manometric recordings of the intrasyrinx pressure in 32 patients including 21 Chiari type 1 patients during syrinx surgery [133]. They recorded the pressure through an 18-gage needle inserted into the syrinx after opening the dura and arachnoid. The recorded pressures ranged from 0.5 to 22.0 cmH2O (mean, 7.7). They described that the patients with syrinx pressures greater than 7.7 cmH2O tended to have more rapid progression of symptoms. Heiss et al. recorded the pressures of the cervical subarachnoid space and the syrinx through 22-gage spinal needles during surgery in 20 patients of syringomyelia with Chiari type 1 malformation [76]. They reported that the syrinx pressure (15 ± 5.8 mmHg) was identical to the cervical subarachnoid pressure (15.1 ± 4.7 mmHg). Relatively larger values of the syrinx pressure in this study compared with the other two studies may be explained by preservation of the spinal subarachnoid space during recordings. They also reported that the CSF compliance (milliliters of CSF per milliliters of mercury) of the spinal subarachnoid space was significantly low in Chiari-syringomyelia patients than normal controls.
Several studies reported the relationship between the intracranial and spinal subarachnoid pressures in Chiari type 1 malformation. Williams reported the pressure dissociation between the intracranial and spinal subarachnoid spaces during Valsalva maneuver [201]. Häckel et al. reported that eight of nine patients with syrinx had a CSF block, while only three of 13 patients without syrinx showed a block by Valsalva maneuver of Queckenstedt test [73]. Using a manometric Queckenstedt test technique, Tachibana et al. demonstrated severe or complete CSF block with neck flexion and no CSF block with neck extension in the patients of syringomyelia with Chiari type 1 malformation [180]. According to the study by Heiss et al., the Valsalva maneuver during surgery failed to produce significant pressure differences between the intracranial and lumbar subarachnoid space in 20 Chiari patients with syringomyelia [76].
From these pressure studies, there is a variety of the degree of the CSF blockade in patients with Chiari type 1 malformation. The intrasyrinx pressure is almost identical to that of the surrounding subarachnoid space. It is unlikely that a simple pressure gradient is the main mechanism of syrinx formation.
Morphometric studies
Posterior fossa size
Morphometric studies on the posterior fossa and neural structures provided quantitative evidences on etiology of Chiari type 1 malformation. The posterior fossa volume was significantly reduced in the patients with Chiari type 1 malformation compared to normal controls [15, 134, 179, 187, 195]. There were some small differences in the results among the morphometric studies. Nishikawa et al. reported that there was no significant difference in the mean posterior crania fossa volume between Chiari type 1 patients and normal controls in adults [142]. However, the volume ratio of the neural structure (the brainstem and cerebellum) and the posterior cranial fossa was significantly larger in the Chiari patients. From the analysis of MRI in 42 pediatric patients with Chiari type 1 malformation, Sgouros et al. reported that there was no significant difference of the posterior fossa volume between the patients with Chiari malformation only and normal controls, but Chiari patients with syringomyelia had a significant smaller posterior fossa volume [172]. Studies measuring the parameters of the posterior fossa such as length of the supraocciput and clivus also showed small posterior fossa in Chiari type 1 malformation [14, 102, 144, 167]. These studies indicate that Chiari type 1 malformation is a disorder of paraxial mesoderm that induces underdevelopment of the occipital bone and overcrowding in the posterior fossa [134, 142]. However, the relationship between the presence of syringomyelia and size of the posterior fossa has not been clarified.
Tonsillar herniation
Chiari malformation has been defined as the descent of the cerebellar tonsil of 3 or 5 mm below the foramen magnum [1, 18]. Degree of tonsillar herniation was reported to be associated with the severity of the brainstem or cerebellar compression symptoms [47, 207]. However, the literature indicated that tonsillar herniation of less than 3 or 5 mm can cause symptoms consistent with syringomyelia with Chiari type 1 malformation [53, 134, 170]. Even the patients without tonsillar herniation showed clinical presentation of syringomyelia with Chiari type 1 malformation [89, 109, 110, 189, 210] and were successfully treated by posterior fossa decompression.
It was also reported that the degree of tonsillar herniation did not correlate with presence of syringomyelia and size of the syrinx [125, 134, 175, 178, 207, 208]. Some studies demonstrated that intermediate level of tonsillar herniation was most frequently associated with syringomyelia. Stevens, et al. reported that syringomyelia was present in 57% of the patients showing the tonsillar descent at occiput-C1, 70% at C1–C2, and 20% at lower than C2 [175]. Stovner, et al. also reported that syringomyelia was significantly more associated with a herniation of 9 to 14 mm (56%) than smaller (13%) or larger (13%) herniations [178]. In a clinical study on surgical series of Chiari type 1 malformation by Yamazaki et al., the length of the ectopic tonsil was significantly larger in the patients without syringomyelia than those with syringomyelia [208].
According to these morphological studies, the role of mechanical effects of the displaced tonsil on the upper cervical cord may be limited.
Effects of surgical treatment
Posterior decompression
Gardner initially reported suboccipital craniectomy with opening of the fourth ventricle and plugging of the obex as a surgical treatment of syringomyelia associated with Chiari type 1 malformation [59]. The rationale of obex plugging was based on the idea that CSF entered into the central canal from the fourth ventricle. The Gardner's operation had been performed by many neurosurgeons [24, 25, 29, 43, 82, 116, 124, 153, 186]. However, simple decompressive procedures at the craniovertebral junction proved to have similar effects on reduction of syringomyelia with lower incidence of complications [56, 121]. Suboccipital craniectomy with laminectomy of the upper cervical spine and expansive duraplasty has been a standard surgery in this disorder [5, 7, 11, 12, 23, 36, 67, 81, 138, 165, 168, 188–192]. Several variations in procedures were reported. The arachnoid membrane was opened to explore the foramen magendie and excise adhesions [10, 31, 32, 39, 48, 63, 64, 71, 103, 107] or was left intact [37, 173, 199]. Some authors left the dura mater open with arachnoid dissection [22, 107] or intact [151]. Displaced tonsils were sometimes manipulated, coagulated or resected [4, 8, 9, 33, 54, 68, 72, 108, 112, 140, 205]. To prevent CSF-related complications, some authors did not open the dura, but removed the dural band (occipitoatlantal membrane) or outer layer of the dura [30, 55, 61, 75, 94, 98, 118, 136, 147, 148, 209, 211]. Meta-analysis of 582 pediatric patients in the literature revealed that foramen magnum decompression without duraplasty was associated with higher risk of reoperation but showed lower risk of complication compared to that with duraplasty [42]. There was no significant difference between these two methods in clinical improvement and reduction of syringomyelia after surgery. Several authors recommended suboccipital expansive craniotomy using autologous bone or synthetic materials to obtain dural expansion [84, 162, 163, 181, 193]. Too wide suboccipital craniectomy was also reported to produce downward displacement of the hindbrain [41, 84]. Thus, enlargement of the subarachnoid space around the hindbrain will be important to provide therapeutic effects. Recent variations in surgical procedures aimed to reduce complications or to achieve sufficient decompression.
Shunting procedures
Shunting procedures such as syringo-subarachnoid (S-S), syringo-peritoneal or syringo-pleural shunting are another option of surgical treatment. Syrinx shunting was developed as an additional procedure to foramen magnum decompression [4, 48, 52, 130, 160, 183, 197] or as a surgical treatment of syringomyelia without hindbrain abnormalities [17, 114, 122, 152, 182, 194]. Several authors reported that S-S shunting was effective in reduction of syrinx and improvement of syringomyeliac symptoms as the primary surgical treatment in syringomyelia with Chiari type 1 malformation [77–79, 92, 93, 96, 97, 149]. Although the syrinx shunting has shown higher incidence of reoperation [19, 171, 202], shunting procedures are the important option for syringomyelia of various etiologies including Chiari type 1 malformation. S-S shunting, which drains the syrinx fluid into the surrounding subarachnoid space, theoretically does not alter the CSF flow around the foramen magnum. The previous theories proposing CSF entrance from the subarachnoid space does not explain why S-S shunting works well as far as the shunt tube is patent.
Pre-syrinx state
In 1999, Fischbein et al. reported 5 patients showing enlarged spinal cord with parenchymal T1 and T2 prolongation but no cavitations on MR imaging, and called this condition as the presyrinx state [50]. Their series included one case of Chiari type 1 malformation. They proposed that the increased CSF pressure by the pulsatile tonsillar descent drives CSF into the spinal cord parenchyma via perivascular spaces. The driven CSF will enlarge the central canal in syringomyelia. If the central canal is not patent, the driven CSF will distribute more diffusely in the spinal cord parenchyma and result in the presyrinx state. Several authors reported similar MR imaging features as the presyrinx state in Chiari malformations [65, 119], trauma [157, 169], arachnoiditis [87], hydrocephalus [137], or posterior fossa arachnoid cyst [143]. The MR appearance may be identical to that in posttraumatic microcystic degeneration [49, 113, 123] or adhesive spinal arachnoiditis [106]. Although the driven mechanism of CSF from the subarachnoid space into the central canal or the spinal cord parenchyma via perivascular spaces should be further verified, explanation for the extracellular fluid accumulation is plausible.
Recently, we investigated MR imaging findings of the spinal cord parenchyma in syringomyelia with Chiari type 1 malformation [2]. Parenchymal hyperintensity areas were present around the central canal and base of the posterior column adjacent to the syringomyelic cavity on T2-weighted images. This study indicates that the elevated extracellular fluid state is commonly present in the spinal cord in syringomyelia with Chiari type 1 malformation (Fig. 1). Such centrifugal pattern of the extracellular fluid accumulation is most likely produced by the disturbed absorption mechanisms of the extracellular fluid, not by the driven force of CSF from the spinal cord surface [2].
MR imaging of the cervical spine in a 16-year-old girl showing syringomyelia with Chiari type 1 malformation. a T1-weighted sagittal image showing displaced tonsil and syringomyelia from the C2/3 to C6/7 levels. b T2-weighted sagittal image demonstrates intramedullary hyperintense areas at the C2 and C7 levels. The three lines indicate the levels of axial slices. c–h T1- (c, e, g) and T2-weighted (d, f, h) axial images at the upper (c, d), middle (e, f), and lower C2 (g, h) levels. T2-weighted images clearly demonstrate hyperintense areas at the central canal and the posterior gray matter (d, f), while T1-weighted images show only slightly hypointense signal (c, e). At the C2/3 level, T2-weighted image (h) demonstrates more extensive abnormal signal area in the spinal cord than T1-weighted image (g)
A new hypothesis for syrinx formation
The evidences of CSF dynamics, pressure studies, morphology of the hindbrain structures, effects of surgical intervention and recent MR imaging findings of “pre-syrinx state” promote new insights into the pathogenesis of syrinx in Chiari type 1 malformation.
Anatomical consideration
Human spinal cord has a characteristic vascular distribution over the cord surface. The outer layer of the pia mater covers the anterior spinal artery and vein at the anterior surface. There are no arachnoid trabeculae in the anterior subarachnoid space. In contrasts, the posterior subarachnoid space contains a longitudinal midline dorsal septum, which becomes only a few strands immediately below the foramen magnum [139]. The posterior spinal veins and arteries are situated in the true subarachnoid space with arachnoid trabeculations [184]. The posterior spinal veins receive venous tributaries from the base of the posterior columns [62, 135] and constitute an important venous drainage of the spinal cord.
In the spinal cord, extracellular fluid is intimately associated with blood circulation. At the capillary level, fluid moves from the blood flow into the interstitial space at the arteriolar end of the capillary, where the filtration pressure exceeds the oncotic pressure, and from the interstitial space into the capillary at the venular end, where the oncotic pressure exceeds the filtration pressure [60]. It has been known that CSF is produced not only at the choroid plexus but also at the brain and spinal cord [129, 166]. Clinical and experimental studies using CTM and tracer techniques indicate that there is a significant fluid communication between the subarachnoid CSF and the extracellular space in the spinal cord. Considering these evidences, the extracellular fluid of the spinal cord contains both the filtrate from the spinal cord microvasculature and the CSF, and at least some part of the extracellular fluid will be absorbed into the intramedullary venous channels (Fig. 2-a).
Schematic presentations of the extracellular fluid circulation in the cervical spinal cord. ASA anterior spinal artery, ASV anterior spinal vein, PSA posterior spinal artery, PSV posterior spinal vein, PCC central canal. a Normal spinal cord. Small arrows indicate the flow of the extracellular fluid. The fluid in the extracellular space is derived from the filtrate of the arteriole end of the capillaries and the subarachnoid space via the perivascular spaces. The central canal acts as the active transport of the fluid. The extracellular fluid is absorbed through the intramedullary venous channels. The posterior spinal veins are situated in the posterior subarachnoid space and are directly influenced by the CSF pressure of the posterior subarachnoid space. b Syringomyelia associated with Chiari type 1 malformation. Reduced compliance of the posterior spinal veins due to the decreased compliance of the spinal subarachnoid space produces disturbed absorption of the extracellular fluid through the intramedullary venous channels. The accumulated extracellular fluid results in the enlarged central canal and the interstitial edema. Cleft formation of the expanded central canal and the accumulated extracellular fluid produce the extracanalicular syrinx
Venous compliance and syrinx formation
The spinal CSF shows pulsatile movement with arterial pulsation. At the foramen magnum level, CSF enters into the spinal CSF space during systole and goes back to the intracranial space during diastole. The spinal CSF space will respond such CSF volume changes by altering the venous blood volume of the spinal cord and/or the epidural venous plexus. These venous blood volume changes during cardiac cycle may help to absorb blood from the capillary bed and the extracellular fluid from the spinal cord parenchyma.
There is evidence that compliance (the volume change per the pressure change) of the spinal CSF space is reduced in syringomyelia with Chiari type 1 malformation [76]. Reduced intracranial compliance determined from cine-mode MR imaging was also reported in Chiari type 1 malformation [3]. The low compliance of the CSF space is most likely produced by the tonsillar blockade of the posterior subarachnoid space at the foramen magnum. Because the posterior spinal veins exist in the true subaracnoid space, the spinal CSF pressure directly influences the posterior spinal veins and will reduce compliance of the posterior spinal veins. That is, the posterior spinal veins reduce the ability to expand during diastole of cardiac cycle and the absorption mechanism of the extracellular fluid from the spinal cord parenchyma will be most likely disturbed. The spinal cord blood flow may be preserved because of the preserved arteriovenous perfusion pressure. Thus, the reduced venous compliance results in decreased absorption of the extracellular fluid through the intramedullary venous channels. Because the central canal acts as the active transport of the fluid, the decreased venous absorption will produce enlargement of the central canal and increased extracellular fluid (interstitial edema) around the central canal (Fig. 2b). The extracellular fluid will be accumulated also in the relatively coarse areas such as the central gray matter and the posterior gray matter. Cleft formation initiated by rupture of the distended central canal may contribute to formation of the extracanalicular syrinx (Fig. 3).
MR imaging of the cervical spine in a 28-year-old woman showing syringomyelia with Chiari type 1 malformation. a Coronal image with fast imaging employing steady-state acquisition (FIESTA). This heavily T2-weighted image clearly demonstrates the enlarged central canal and the extracanalicular extension of the syrinx (arrow). b–e T1- (b, d) and T2-weighted (c, e) axial images at the C4/5 (b, c) and C5/6 (d, e) levels. Abnormal hyperintense areas around the central canal (c) or the syrinx (e) indicate accumulation of the extracellular fluid or interstitial edema
Spinal dural arteriovenous fistula (AVF) also shows venous congestion and the spinal cord edema, but syringomyelia is uncommon. This should be noted. Spinal dural AVF produces significant decrease in spinal cord perfusion pressure. The abnormal perfusion state will result in both the extracellular fluid accumulation and intracellular edema caused by ischemia. Such ischemic edematous state will not result in syringomyelic cavity. Accumulation of the extracellular fluid with the preserved perfusion pressure may be important in expansion of the fluid pathways in the spinal cord.
Although most of our supposed mechanisms lack the experimental or clinical evidences and consist of speculations, this decreased absorption hypothesis can explain several radiological and clinical features. For example, delayed visualization of syringomyelia by CTM is the result of delayed clearance of the contrast via the intramedullary veins after influx of the subarachnoid contrast into the syrinx via the perivascular spaces. S-S shunting drains the syrinx fluid (the accumulated extracellular fluid) into the subarachnoid space where the usual CSF circulation and absorption mechanisms exist. It is still unclear why some patients with Chiari type 1 malformation develop syringomyelia and some do not. Differences in capacity of the venous absorption of the extracellular fluid or the fluid transport mechanism of the central canal may underlie such variation in clinical presentation of Chiari type 1 malformation.
Conclusions
This study critically reviews the evidences of the clinicopathological, radiological and clinical presentations of syringomyelia associated with Chiari type 1 malformation. The previous theories for the pathogenesis do not fully explain the radiological features and effects of surgical treatment such as shunting procedures. The MR appearance of syringomyelia demonstrates the extracellular fluid accumulation in the spinal cord parenchyma and suggests decreased absorption mechanisms of the extracellular fluid. The review of the evidences promotes a new hypothesis of syrinx formation: Reduced compliance of the posterior spinal cord veins, that is associated with the decreased spinal CSF compliance due to the foramen magnum blockade, will produce disturbed absorption of the extracellular fluid through the intramedullary venous channels and result in syringomyelia in Chiari type 1 malformation.
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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.
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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.
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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
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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
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DOI: https://doi.org/10.1007/s10143-010-0266-5