Introduction

Chiari type I malformation, characterized by downward herniation of the caudal cerebellum or medulla oblongata into the foramen magnum, is one of the major causes of syringomyelia [1, 2]. Although various surgical procedures to restore cerebrospinal fluid (CSF) circulation and decompress the neuraxis have been described, there is no consensus regarding the optimal surgical procedure. Some authors prefer foramen magnum decompression (FMD) with dural opening [3, 4], whereas others believe that duraplasty [5–8], sometimes with tonsillectomy [9–12], is required to expand the posterior fossa and restore normal CSF flow. Syringosubarachnoid shunt is also used either alone [13, 14] or combined with FMD [11, 15].

We prospectively investigated the results of our surgical method, FMD combined with C1 laminectomy and excision of the outer layer of the dura mater, which was advocated by Isu et al. [16] and is recognized as a minimally invasive surgical technique for the spinal cord. The goals of this surgical procedure are to correct the circulatory disturbance of CSF at the foramen magnum and create a new cisterna magna, considering the dural inner part capability of expansion. So far, there are few reports applying this surgical procedure as a single method. Gambardella et al. [17] performed the surgery for eight patients with syringomyelia and focused on surgical techniques. The other published reports were from the same institution and focused on the scoliosis, cervical spinal motion, and neuropathic pain [18–20], respectively. The objectives of our study were to assess surgery-related results and identify factors influencing improvement by comparing symptoms, clinical results, and imaging findings.

Materials and methods

Twenty patients underwent surgery at our hospital between 2000 and 2010 for syringomyelia associated with Chiari type I malformation. There were two male and 18 female patients, ranging in age from 11 to 57 years (mean 31.0 years) at the time of surgery. Patients with syringomyelia associated with other diseases, such as spinal cord tumors or adhesive arachnoiditis, or those with spinal cord injuries, were excluded from this study. All patients underwent FMD combined with C1 laminectomy and excision of the outer layer of the dura mater. The postoperative period ranged from 1.3 to 10.8 years (mean 6.0 years). After surgery, patients in whom the size of the syrinx decreased on both sagittal and axial magnetic resonance imaging (MRI) were defined as the decreased group, and those in whom the size was relatively unchanged were defined as the unchanged group (Fig. 1). The following parameters were compared between groups: age at the time of surgery, duration of morbidity (from symptom onset to initial surgery), improvement of preoperative symptoms, type and length of the syrinx, subarachnoid space at the foramen magnum level in postoperative MRI (Fig. 2), basal and clivo-axial angles, cervical alignment from C2 to C7, and presence or absence of scoliosis in preoperative radiographs. Scoliosis was defined as a Cobb angle ≥10°.

Fig. 1
figure 1

Representative pre- and postoperative T2-weighted magnetic resonance (MR) images from patients in the decreased and unchanged group. Note the markedly decreased size of the syrinx in a, b in contrast to the unchanged size in c, d

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Fig. 2
figure 2

Representative pre- and postoperative T2-weighted magnetic resonance (MR) images. a, b Note that the subarachnoid space at the level of the foramen magnum expanded after surgery in the decreased-group patient (arrowheads). c, d This is in contrast to residual narrowing of the subarachnoid space in the patient in the unchanged group

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Clinical results were evaluated on the basis of the outcome scale proposed by Bidzinski [21] (Table 1).

Table 1 Outcome scale for syringomyelia proposed by Bidzinski [21]
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Syrinx morphology was classified into three types—central, enlarged, and deviated—based on axial MRI at the level corresponding to the dermatomal distribution of sensory disturbance and at the level where syrinx size was the greatest in asymptomatic scoliotic patients (Fig. 3) [22].

Fig. 3
figure 3

Classification of syrinx type. Syrinx morphology was classified into three types—central, enlarged, and deviated—based on axial magnetic resonance (MR) images obtained at the level at which syrinx size was maximum

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Statistical analysis

The Mann–Whitney U test was used to compare data between groups. Chi-square test for independence was used to evaluate clinical results, syrinx type, presence or absence of scoliosis, and enlarged subarachnoid space after surgery. Statistical significance was defined as a probability value <0.05. Values are presented as mean ± standard deviation (SD).

Statement of ethics

All applicable institutional and governmental regulations concerning the ethical evaluation of our patients were followed during the course of this research. This study was approved by the Institutional Review Board of School of Medicine, Keio University. We obtained signed consent forms from all patients.

Results

After surgery, syrinx size decreased in 11 patients (decreased group) and remained relatively unchanged in nine (unchanged group). Initial symptoms were segmental dysesthesia in 11 patients, numbness in 11, radicular pain in seven, and upper-extremity weakness in one. Two patients with scoliosis, whose syringomyelia was discovered and diagnosed by MRI, had no symptoms. Clinical results were analyzed in the 18 patients presenting with obvious symptoms. Following Bidzinski’s [21] outcome scale, of the ten patients in the decreased group, four were classified as very good and six as good. In contrast, in the unchanged group, only one patient was classified as good and seven were classified as poor (Table 2). The difference in clinical outcomes between groups was significant (p < 0.01), suggesting that a reduction in syrinx size is correlated with clinical improvement. There were no complications, such as CSF collection in the operative wound, pseudomeningocele, or meningitis, in either group.

Table 2 Clinical results for the two groups
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There was no significant difference in age at the time of surgery between groups (Table 3). Average morbidity duration was analyzed for the 18 symptomatic patients, excluding two scoliotic patients whose symptoms from syringomyelia were not obvious. The decreased group had suffered from syringomyelia for 14.1 months and the unchanged group for an average of 43.5 months. This difference in mean morbidity duration between groups was significant (Table 3), suggesting there could be a correlation between longer morbidity and unchanged syrinx size following surgery.

Table 3 Comparison of patient characteristics
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Analysis of morphological features of preoperative syrinxes revealed that five patients in the decreased group had the central type of syrinx, whereas six had the enlarged type (Table 4). Of the nine patients in the unchanged group, six had a deviated syrinx and three an enlarged syrinx. The differences in morphology of preoperative syrinx between groups were significant, with patients in the decreased and unchanged groups having central and deviated syrinxes, respectively.

Table 4 Preoperative syrinx morphology
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The average length of the preoperative syrinx was significantly shorter in the decreased group (9.5 vs 14.3 vertebral bodies) (Table 3). Notably, syrinx length in all patients in the unchanged group was more than ten vertebral bodies (Fig. 4). These results suggest that FMD might be a good indication for syringomyelia shorter than ten vertebral bodies.

Fig. 4
figure 4

Comparison of syrinx length between groups

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Postoperative subarachnoid space at the foramen magnum was enlarged in every member of the decreased group, whereas residual narrowing was observed in four of the nine patients in the unchanged group, with a statistically significant intergroup difference (Table 3). In contrast, there were no significant differences in basal or clivoaxial angles, cervical alignment from C2 to C7, or presence or absence of scoliosis in preoperative radiographs between groups (Table 3). In the unchanged group, a syringosubarachnoid shunt was later performed in seven of the nine patients. Average duration between FMD and shunt was 16.3 months (range 6–24 months). Because there are some cases in which syrinxes gradually decrease after FMD, we wait for approximately 12 months before performing the second operation. After shunt treatment, the size of all syrinxes decreased, and patients’ symptoms were relieved. The other two patients underwent conservative treatment consisting solely of medication. Although these two patients showed slight improvement, their syrinx size remained unchanged, and they continued to experience symptoms such as numbness and dysesthesia.

Discussion

We performed FMD with excision of the outer layer of the dura mater in patients with syringomyelia due to Chiari type I malformation and prospectively examined the factors contributing to the surgical outcome. After the surgery, 55 % of patients showed an improvement in clinical symptoms, along with a decrease in syrinx size. Clinical symptoms of the other patients did not improve, and there was no change in syrinx size. Patients with deviated syrinx, a long syrinx, and a long duration of morbidity showed a poor prognosis after FMD. Furthermore, patients had a poor prognosis when postoperative MRI showed residual narrowing of the subarachnoid space. Thus, the ability of this surgical procedure to improve clinical symptoms is not consistent, being dependent upon the underlying pathogenesis of the syringomyelia. Considering that the condition of most patients with an unchanged syrinx size was improved by additional procedures, such as syringosubarachnoid shunt, we conclude that the choice of surgical procedure for each pathological condition is critical for the effective treatment of the syringomyelia in Chiari type I malformation.

These results suggest that syrinx size can be reduced by FMD in patients with a shorter morbidity duration and a short syrinx (<10 vertebral bodies) and of the central type. In agreement with our results, previous studies demonstrated that these factors contribute to clinical improvement after this surgical procedure [9, 18, 23, 24]. In contrast to the occasional report of postoperative complications, such as CSF collection in the operative wound, pseudomeningocele, or meningitis, when FMD was used with dural opening or duraplasty [3–6, 9, 10, 12, 15], there is no risk of such complications when FMD is used with excision of the dural outer layer [16–18]. Furthermore, previous reports demonstrated that FMD without duraplasty has a lower risk of complications than that with duraplasty [25, 26]. Therefore, treatment consisting of FMD with excision of the outer dural layer may provide optimal benefit with a low risk of postoperative complications if the patient has the prognostic factors for improvement.

Few studies have demonstrated a relationship between syrinx morphology and postoperative results in patients with Chiari type I malformation. In this study, treatment with FMD produced both clinical improvement and a smaller syrinx in all patients with a central syrinx. Similar to these results, previous studies demonstrated that patients with the central type of syrinx rather than the deviated type tend to recover well from preoperative neuropathic pain after surgery [20, 23]. Milhorat et al. [22, 27] demonstrated that the central syrinx is anatomically continuous with the fourth ventricle. Therefore, decompression at the level of the foramen magnum for this type of syrinx is a reasonable approach for releasing an obstruction in CSF circulation and allowing communication between syrinx and the fourth ventricle. In contrast, we found that FMD did not reduce the syrinx size for all patients with the deviated type. This form of syrinx originates in the gray or white matter of the parenchyma and does not communicate with the central canal [27]. The deviated syrinx is thought to be produced by cleft formation and extracellular fluid accumulation in the parenchyma [28]. Thus, even if the CSF circulation at the level of the foramen magnum recovers following FMD, the deviated syrinx, which separates from the central canal, does not decompress and remains unchanged. Because patients in this study with a deviated syrinx experienced improvement after undergoing an additional operation (syringosubarachnoid shunt), direct decompression using a shunt may be adequate treatment for this syrinx type. Intriguingly, Hida et al. [14] placed a syringosubarachnoid shunt in patients as the initial treatment and reported no case of shunt malformation after shunt tube insertion into the ventral subarachnoid space. Although there are no other reports in which this procedure was followed, the syringosubarachnoid shunt alone may be an appropriate surgical choice for improving syringomyelia. In regard to cases with an enlarged syrinx reviewed in this study, surgical outcomes of FMD were not consistent. Therefore, for such cases, other prognostic factors, including symptom duration and syrinx length should be taken into account when determining the surgical indication of FMD or syringosubarachnoid shunt.

In this study, 44 % of patients with an unchanged syrinx size had residual narrowing of the subarachnoid space in the cerebellomedullary cistern after surgery, necessitating additional surgery. These results indicated that an adhesive arachnoiditis concomitantly developed at the level of the foramen magnum. In fact, Alfieri and Pinna [9] pointed out the existence of adhesive arachnoiditis at the level of the foramen magnum in visual inspection during duraplasty. Aghakhani et al. [5] reported surgical outcomes of Chiari-related syringomyelia and demonstrated that one factor associated with poor outcome was arachnoiditis. They also showed that the presence of arachnoiditis was associated with poor clinical presentation [5]. Previous reports demonstrated that FMD without duraplasty is associated with a higher risk of reoperation compared with that with duraplasty [26]. Although the reported risk of complications, including CSF leakage or meningitis, ranges from 2.7 % to 36 % [5, 6, 9, 10, 12, 15], FMD with duraplasty could be an appropriate choice for releasing subarachnoid space adhesion. Alternatively, syringosubarachnoid shunt could be considered as a means by which to directly decompress the syrinx, regardless of adhesive arachnoiditis at the level of the foramen magnum [13, 14]. Further studies are needed to determine the most suitable surgical procedures for treating adhesive cisterna associated with syringomyelia.

Previous studies demonstrated that Chiari patients with syringomyelia have a significantly smaller foramen magnum volume than control individuals [29]. These results indicate that the Chiari type I malformation is a disorder of the paraxial mesoderm that induces underdevelopment of the occipital bone and overcrowding in the posterior fossa [28]. In this study, our comparison of bone morphological factors, such as scoliosis, cervical alignment, and angles around the foramen magnum, revealed no significant differences between patients with a decreased versus an unchanged syrinx size. In agreement with our results, Ono et al. [18] compared the decrease in syrinx size after FMD in scoliotic versus nonscoliotic patients and found no statistically significant intergroup difference. Taken together, results of our study suggest that decreased or unchanged syrinx size after surgery is not affected by a mesodermal abnormality but by syrinx morphology or choice of surgical technique.

Conclusion

In patients with syringomyelia associated with Chiari type I malformation, this study showed that: (1) a longer length and (2) laterally deviated syrinx, (3) a longer morbidity duration, and (4) postoperative residual narrowing of the subarachnoid space in the cerebellomedullary cistern are prognostic factors for an unchanged syrinx size following FMD. The pathogenesis of syringomyelia in Chiari type I malformation is not consistent, and the choice of surgical technique for each pathological condition is important.