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Long-Term Outcomes After Small-Bone-Window Posterior Fossa Decompression and Duraplasty in Adults with Chiari Malformation Type I
Accepted Manuscript Long-term outcomes following small-bone-window posterior fossa decompression and duraplasty in adults with Chiari malformation type I Xiaofeng Deng, M.D, Chenlong Yang, M.D, Jiahe Gan, M.D, Liang Wu, M.D, Tao Yang, M.D, Jun Yang, M.D, Yulun Xu, M.D., Ph.D PII:
S1878-8750(15)00083-2
DOI:
10.1016/j.wneu.2015.02.006
Reference:
WNEU 2715
To appear in:
World Neurosurgery
Received Date: 6 October 2014 Revised Date:
1 February 2015
Accepted Date: 4 February 2015
Please cite this article as: Deng X, Yang C, Gan J, Wu L, Yang T, Yang J, Xu Y, Long-term outcomes following small-bone-window posterior fossa decompression and duraplasty in adults with Chiari malformation type I, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.02.006. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1 Abstract Background:
Small-bone-window
posterior
fossa
decompression
(SPFD)
with
duraplasty is one of the popular surgical options for Chiari malformation type I (CMI), but
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its efficacy is controversial and the risk factors of clinical outcome remain unclear. Methods: The study cohort included 152 CMI patients who received SPFD at Beijing Tiantan hospital from January 2008 to September 2009. All the patients underwent combined surgical procedures: a small-bone-window sub-occipital decompression (diameter, 2.5-3cm) and a C1 laminectomy (1.5-2cm wide) followed by a duraplasty with
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an autologous graft. Clinical manifestations, radiological features and follow-up data over a six-year span were analyzed. Risk factors associated with outcome were investigated
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using chi-square analysis and logistic regression analysis.
Results: The average follow-up duration was 74 months. Symptoms were improved in 126 patients (82.9%), remained stable in 21 patients (13.8%), and deteriorated in 5 patients (3.3%). There was no mortality. Postoperative magnetic resonance (MR) images were available in all patients. Preoperatively 112 patients were associated with syringomyelia (SM), and the follow-up MR images showed obvious reduction of SM in 73 patients (65.2%) and no significant change in 39 patients (34.8%). Additionally, cistern
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magna enlargement was observed in 92 patients (85.2%). Regression analysis indicates preoperative motor dysfunction, brainstem herniation and basilar invagination may influence the clinical outcome (p<0.05).
Conclusions: Small-bone-window posterior fossa decompression with duraplasty is an
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effective and safe treatment option with a low complication rate. Motor dysfunction,
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brainstem herniation and basilar invagination are predictors of poor clinical prognosis.
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Title Page Long-term outcomes following small-bone-window posterior fossa
Xiaofeng Deng *, a, M.D. Chenlong Yang *, a, M.D.
Liang Wu a, M.D.
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Tao Yang a, M.D.
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Jiahe Gan b, M.D.
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decompression and duraplasty in adults with Chiari malformation type I
Jun Yang a, M.D.
Yulun Xu a, M.D., Ph.D.
* Xiaofeng Deng and Chenlong Yang contributed to the work equally and should be
a
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regarded as co-first authors.
Department of Neurosurgery, China National Clinical Research Center for Neurological
Diseases, Beijing Tiantan Hospital, Capital Medical University, No. 6 Tiantan Xili, Dongcheng District, Beijing 100050, China.
School of Clinical Medicine, Capital Medical University, No. 10 Xitoutiao, Youanmen,
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b
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Fengtai District, Beijing 100069, China.
Correspondence to: Prof. Yulun Xu, M.D., Ph.D. Tel: +86-13501285331, fax: +86-10-6709-6523; E-mail: [email protected]
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Introduction Chiari malformation (CM), also known as Arnold-Chiari malformation, is a congenital malformation characterized by a downward displacement of the cerebellar tonsils into the spinal canal (9, 22). CM can be divided into four types, in which Chiari malformation
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type I (CMI) is the most common. The mechanism of CM remains unclear, and the majority of scholars support the view that it is resulting from the reduced capacity of the posterior cranial fossa, which has been demonstrated by studies on the morphology of posterior cranial fossa (4, 9, 20). CM may be complicated by a variety of other
invagination, occipitalization and scoliosis (8).
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malformations, including syringomyelia (SM), hydrocephalus, platybasia, basilar
Regarding the treatment of CMI, most authors agree that posterior fossa
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decompression can lead to both clinical and radiological improvement (10, 13, 23, 2729). However, specific surgical procedures remain controversial, such as craniectomy and bone-window size, whether the arachnoid should be opened and whether cerebellar tonsil should be manipulated (13, 19, 26, 27, 32). Besides, the risk factors on prognosis are still ambiguous.
The current study aims to evaluate the efficacy of small-bone-window posterior fossa decompression (SPFD) with duraplasty in the treatment of CMI, and to analyze the
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related predictors of poor outcome. Materials and methods
The study was approved by the Institutional Review Board and Ethics Committee of
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Beijing Tiantan Hospital, Capital Medical University. The cohort included 152 CMI patients who received SPFD in our department from January 2008 to September 2009.
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Exclusion criteria included (a) occipitocervical instability; or (b) incomplete data. Clinical presentations
Clinical symptoms and physical examinations were recorded, including headache, sensory-motor disturbance, and muscle atrophy. The main clinical manifestations were classified into five groups: 1) sensory disturbance, including numbness, and deficits of pain and temperature sensation, 2) motor dysfunction, including weakness of limbs and muscle atrophy, 3) head and/or neck pain, 4) extremity and/or trunk pain, 5) other neurological disorders, including diplopia, tinnitus, hoarseness, cough, dysphagia, ataxia, and nausea or vomiting.
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Imaging Preoperative magnetic resonance (MR) imaging of the cervical spine was performed on all patients. The descending distance between the inferior pole of the cerebellar tonsil and level of the foramen magnum was measured on sagittal T1-weighted images. The
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degree of cerebellar descent was classified into three groups based on the cerebellar tonsil descent (CTD) grading scale: 1) Grade I, the tonsil descends over the foramen magnum but does not reach the C1 arch; 2) Grade II, the tonsil descends to C1 arch level; 3) Grade III, the tonsil descends below the C1 arch.
The location of SM was determined in sagittal MR images and it was classified
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into cervical, cervicothoracic and holocord syrinx. Other associated abnormalities were also recorded, such as ventricular dilation, scoliosis, basilar invagination, occipitalization
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and Klippel-Feil syndrome. Ventricular dilation was defined as Evans’ index >0.30 (3) and scoliosis was defined as the curve angle ≥10º according to the Cobb method (7, 11, 21, 25). Surgical approach
Small-bone-window posterior fossa decompression with duraplasty was performed on all patients. After patients were left-lateral positioned, a posterior midline skin incision was
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made from 1cm below the inion to the spinous process of C4 and an autologous graft (2cm×2cm) was resected from the fascia and reserved. A SPFD procedure including a small-bone-window
sub-occipital
craniectomy
(diameter,
2.5-3cm)
and
a
C-1
laminectomy (1.5-2cm) was performed. The thick and constraining dural band found at
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the occipital-cervical junction was resected. The dura mater was opened with the arachnoid intact, and then the dura mater was grafted with the autologous graft to enlarge the cistern magna.
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Besides, 28 patients in the cohort underwent intraoperative ultrasound examinations. The volume of subarachnoid space around the tonsils was measured both before dura mater incision and after grafting. Doppler ultrasound diagnostic system (GE Logiq 5) was used (5~8 MHz, probe size 8mmx15 mm). Prior to dura mater incision, the bone window was filled with sterilizing saline, and epidural detection was performed putting the probe close to the dura mater. Ultrasonography showed disappearance of the cisterna magna (Fig. 3c). After duraplasty with autologous fascia, epidural detection was repeated. The enlargement of the subarachnoid space (≥ 3mm) and the reconstruction of cisterna magna could confirm the efficiency of decompression (Fig. 3d).
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Follow-up Follow-up data for all patients were obtained during individual office visits or telephone interviews. MR imaging was performed postoperatively, at discharge, and semi-annually or annually thereafter. The clinical outcomes were categorized as follows: 1) Improved:
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the patients experienced a partial or complete relief of their symptoms or neurological examination showed observable improvement. 2) Not improved: Slight or no change in symptoms, or worsening of their clinical status. The clinical symptoms and neurological functions were assessed independently by two neurosurgeons, reviewed and processed
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by another evaluator. Statistical evaluation
SPSS 18.0 software (SPSS Inc., Chicago, IL, USA) was used for statistical analyses.
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Chi-square test was used to screen the potential risk factors, including gender, age at onset, age at diagnosis, duration of symptoms, main clinical presentations, CTD grades, syringomyelia, hydrocephalus, brainstem herniation, basilar invagination, and scoliosis. Furthermore, logistic analysis was performed to identify the risk factors on prognosis. Probability (p) values ≤0.05 were considered significant. Results
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Patient population and clinical characteristics From January 2008 through September 2009, 158 consecutive CMI patients underwent SPFD in our department. Six patients were lost to follow-up and excluded; a total of 152 patients were enrolled in the study. There were 52 males and 100 females, with a male-
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to-female ratio of 1:1.92. The average age at time of surgery was 39.2 ±11.7 years (range 18 to 60 years). Ages at onset ranged from 7 to 58 years (mean 33.1 ±11.2
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years). The duration of symptoms ranged from 1 to 420 months (mean 66 months; median 36 months). According to the main clinical-manifestation categorization, 39 patients had motor dysfunction, 59 patients had sensory disturbance, 13 patients had head and/or neck pain, 10 patients had extremity and/or trunk pain, and 31 patients had other neurological disorders. The main clinical manifestations were summarized in table 1. Preoperative imaging The distance of tonsillar herniation ranged from 5.0 to 27.0 mm (mean 9.4 ±4.8mm). According to the CTD grading criteria, 72 patients (47.4%) were identified with Grade I 4
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(Fig. 1a), 53 patients (34.9%) with Grade II (Fig. 1b), and 27 patients (17.7%) with Grade III (Fig. 1c). Concomitant SM was observed in 112 patients (73.7%): 18 (16.1%) with a cervical syrinx, 86 (76.8%) with a cervicothoracic syrinx and 8 (7.1%) with a holocord
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syrinx. The other disorders associated with CMI were summarized in Table 2. Complications and follow-up
Meningitis occurred in seven patients after operation, and all were effectively controlled by antibiotics and lumbar drainage. One patient developed cerebrospinal fluid (CSF) leak, which was resolved following conservative treatment. There was no mortality in this
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cohort. Follow-up data for all patients were available, with a mean duration of 74 months. Symptoms were improved in 126 patients (82.9%), remained unchanged in 21 patients (13.8%), and deteriorated in 5 patients (3.3%). Patients with motor dysfunction showed a
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significantly lower improvement rate (64.1%) than the other groups. The clinical outcomes during follow-up period were summarized in Table 1. Moreover, with regard to the preoperative MR features, patients with brainstem herniation showed a lower improvement rate (68.4%) than those without brainstem herniation (87.7%), and patients with basilar invagination also showed a lower improvement rate (58.8%) than patients without basilar invagination (85.9%).
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On admission, 112 patients were observed with concomitant SM. According to the follow-up MR images, SM disappeared or obviously reduced in 73 patients (65.2%, Fig. 1), and remained stable in the other 39 patients (34.8%). Cistern magna enlargement was observed in 92 patients (85.2%, Fig. 1a, d).
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Logistic analysis indicates motor dysfunction (p=0.006; OR=3.723; 95% CI, 1.467-9.452), brainstem herniation (p=0.026; OR=2.930; 95% CI, 1.135-7.562) and basilar invagination (p=0.038; OR=3.480; 95% CI, 1.071-11.311) had significant effects
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on poor clinical outcomes. Discussion
A popular hypothesis concerning the pathogenesis of CMI is that the hindbrain tissues are dislocated into the spinal canal due to an overcrowded posterior cranial fossa which is caused by the underdevelopment of the mesodermal occipital somite (9, 31). Concerning the formation of SM associated with CMI, there are several different hypotheses. While most of the authors agree the partial obstruction in the foramen magnum area, which blocks the normal circulation of CSF, is the pacing factor in the development of SM (16, 24). Thus, the optimal treatment for CMI should be enlarging 5
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the posterior cranial fossa and relieving the obstruction of CSF flow at the level of foramen magnum. Overall, SPFD can be an effective approach to treat CMI and SM. Surgical procedures of SPFD
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The size of bone window for posterior fossa decompression is under debate (1, 18). A large-bone-window posterior fossa decompression is effective to enlarge the posterior cranial fossa and to relieve the symptoms. However, there might be a higher incidence of complications, such as CSF leak, pseudo cyst, meningitis, and hydrocephalus (5). Besides, excessive removal of the squamous part of the occipital bone could lead to the
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downward and backward displacement of the cerebellum and brainstem, resulting in pseudocephalocele (cerebellum encephalocele from the bone window); thereby further
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obstructing the CSF flow and pulling the trigeminal, abducent, acoustic nerves and lower cranial nerves, leading to a succession of long-term complications. Furthermore, according to the previous studies (5, 6, 9, 15), a small-bone-window craniectomy is sufficient to achieve favorable clinical outcomes and the incidence of complications is obviously reduced. This procedure can not only relieve the compression of the occipitocervical bones, but can also preserve enough bones to support the cerebellum and brainstem. In the current study, all patients underwent a small-bone-window
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approach and high rates of clinical (82.9%) and radiological (85.2%) improvement were achieved. In the long-term follow-up period, no patient developed cerebellar ptosis or hydrocephalus.
Whether it is necessary to open the arachnoid space is another point of
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contention. Some authors believe that CSF-related complications, such as CSF leak and meningitis, are directly associated with the opening of arachnoid (23). The other authors indicate that the incidence of CSF leak does not increase in the arachnoid opening
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group as long as watertight duraplasty is performed, and reconstruction of the cistern magna and tonsillar manipulation could contribute to a better prognosis (2). In our experience, arachnoid opening was not necessary for most patients. SPFD and duraplasty without arachnoid incision is sufficient to relieve the compression and to improve clinical symptoms, and the incidence of CSF-related complications is low in our cohort. Besides, intraoperative ultrasound can be used to verify a satisfactory decompression manifested by increased subarachnoid space around the tonsils and tonsillar pulsation. In the present study, 28 patients underwent intraoperative ultrasound and all of them showed cistern magna enlargement (Fig. 3c, d), which demonstrates a 6
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SPFD and duraplasty without arachnoid incision can effectively relieve the compression at the level of the foramen magnum. Some authors point out that patients receiving herniated tonsil excision experienced better outcomes than patients without tonsillar manipulation, and thus
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attempts should be made to remove the herniated tonsils (5). However, the clinical and radiological results in our study were similar to the reported prognosis of other series in which tonsillar manipulation was performed (2, 5). Additionally, we found the herniated tonsil could shift upward after SPFD with duraplasty in most cases (85.2%) even if it was not manipulated (Fig. 1a, d), and the previous study had also demonstrated that the
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cerebellar tonsils and brainstem could undergo a gradual recovery to normalcy after decompression without tonsillar coagulation in most patients (12). This might result from
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the morphological plasticity of the brain tissues. The tonsillar herniation is generated by the overcrowding of the posterior cranial fossa, and after the capacity of the posterior cranial fossa is enlarged following SPFD, the herniated tonsils could move upward and return to the posterior cranial fossa. It may be unnecessary to manipulate the herniated tonsils for most CMI patients (Chiari malformation type 1.5 might be exceptions). Risk factors on prognosis
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The risk factors on prognosis are still in its infancy. Some authors indicate that ages at time of surgery and symptom duration are significantly associated with prognosis (2). And some studies also consider that age of onset is of vital importance (23). In the current study, a large cohort of 152 patients was enrolled and multivariate analysis was
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performed focusing on ten different factors. Regression analysis showed that the crucial clinical predictors of poor outcome were motor dysfunction, brainstem herniation and basilar invagination.
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According to the main manifestation categories, patients with motor dysfunction
revealed a lower recovery rate than the others, suggesting the impairment of the motor system was difficult to restore. Neurosurgeons may consider that patients whose chief complaints are muscle weakness and muscle atrophy may not respond well to decompression.
CMI along with brainstem herniation is also referred to Chiari malformation type 1.5 (CM 1.5) (14, 30). It is reported that there is no specific sign or symptom peculiar to CM 1.5, but the incidence of unresolved SM after SPFD is nearly two-fold higher in CM 1.5 than CMI. For CM 1.5 patients, a routine SPFD may not be sufficient to decompress
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the cerebella and brainstem, and a more aggressive surgical strategy might be needed to alleviate SM, including bone-window enlargement, arachnoid incision, manipulation of arachnoid adhesions and tonsillectomy. This study demonstrated that it was more difficult to relieve the symptoms and to reduce the syrinx size (Fig. 2) for CM 1.5 patients
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compared with CMI patients. The optimal procedure for CM 1.5 still needs further research.
Basilar invagination was also significantly associated with poor outcomes. For patients with basilar invagination, a pure SPFD may not be enough to relieve the compression on brainstem and cerebellum, especially the ventral compression from the
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odontoid tip. As some authors suggested in the literature, a ventral cervicomedullary junction decompression could be attempted in these cases (17).
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Limitations
For ethical and security considerations, there is no control group with large-bone-window posterior fossa decompression, or control group with arachnoid opening in this study. Conclusions
Small-bone-window posterior fossa decompression with duraplasty is an effective and safe treatment option with a low complication rate. Motor dysfunction, brainstem
Acknowledgments
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herniation and basilar invagination are predictors of poor clinical prognosis.
We thank all of the patients who trusted us with their care, and all of the physicians and
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staff who helped in this study. Conflict of interest
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The authors have no conflicts of interest to disclose.
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References
Abd-El-Barr M, Groff MW: Less is more: limiting the size of posterior fossa decompressions in Chiari I malformations. World Neurosurg. 81:706-707, 2014.
2.
Alfieri A, Pinna G: Long-term results after posterior fossa decompression in syringomyelia with adult Chiari Type I malformation. J Neurosurg Spine. 17:381387, 2012.
3.
Ambarki K, Israelsson H, Wahlin A, Birgander R, Eklund A, Malm J: Brain ventricular size in healthy elderly: comparison between Evans index and volume measurement. Neurosurgery. 67:94-99; discussion 99, 2010.
SC
RI PT
1.
M AN U
4. Aydin S, Hanimoglu H, Tanriverdi T, Yentur E, Kaynar MY: Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surg Neurol. 64:237-241; discussion 241, 2005. Bao C, Yang F, Liu L, Wang B, Li D, Gu Y, Zhang S, Chen L: Surgical treatment of Chiari I malformation complicated with syringomyelia. Exp Ther Med. 5:333-337, 2013.
6.
Batzdorf U, McArthur DL, Bentson JR: Surgical treatment of Chiari malformation with and without syringomyelia: experience with 177 adult patients. J Neurosurg. 118:232-242, 2013.
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5.
EP
7. Brockmeyer D, Gollogly S, Smith JT: Scoliosis associated with Chiari 1 malformations: the effect of suboccipital decompression on scoliosis curve progression: a preliminary study. Spine. 28:2505-2509, 2003.
9.
10.
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8. Colombo LF, Motta F: Consensus conference on Chiari: a malformation or an anomaly? Scoliosis and others orthopaedic deformities related to Chiari 1 malformation. Neurol Sci. 32 Suppl 3:S341-343, 2011. Dagtekin A, Avci E, Kara E, Uzmansel D, Dagtekin O, Koseoglu A, Talas D, Bagdatoglu C: Posterior cranial fossa morphometry in symptomatic adult Chiari I malformation patients: comparative clinical and anatomical study. Clin Neurol Neurosurg. 113:399-403, 2011. El-Ghandour NM: Long-term outcome of surgical management of adult Chiari I malformation. Neurosurg Rev. 35:537-546; discussion 546-547, 2012.
11. Eule JM, Erickson MA, O'Brien MF, Handler M: Chiari I malformation associated with syringomyelia and scoliosis: a twenty-year review of surgical and nonsurgical treatment in a pediatric population. Spine. 27:1451-1455, 2002.
9
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12. Heiss JD, Suffredini G, Bakhtian KD, Sarntinoranont M, Oldfield EH: Normalization of hindbrain morphology after decompression of Chiari malformation Type I. J Neurosurg. 117:942-946, 2012. Imperato A, Seneca V, Cioffi V, Colella G, Gangemi M: Treatment of Chiari malformation: who, when and how. Neurol Sci. 32 Suppl 3:S335-339, 2011.
14.
Kim IK, Wang KC, Kim IO, Cho BK: Chiari 1.5 malformation : an advanced form of Chiari I malformation. J Korean Neurosurg Soc. 48:375-379, 2010.
15.
Klekamp J: Surgical treatment of Chiari I malformation--analysis of intraoperative findings, complications, and outcome for 371 foramen magnum decompressions. Neurosurgery. 71:365-380; discussion 380, 2012.
16.
Koyanagi I, Houkin K: Pathogenesis of syringomyelia associated with Chiari type 1 malformation: review of evidences and proposal of a new hypothesis. Neurosurg Rev. 33:271-284; discussion 284-285, 2010.
17.
Menezes AH: Craniovertebral junction abnormalities with hindbrain herniation and syringomyelia: regression of syringomyelia after removal of ventral craniovertebral junction compression. J Neurosurg. 116:301-309, 2012.
18.
Menezes AH: Current opinions for treatment of symptomatic hindbrain herniation or Chiari type I malformation. World Neurosurg. 75:226-228, 2011.
19.
Milhorat TH, Bolognese PA: Tailored operative technique for Chiari type I malformation using intraoperative color Doppler ultrasonography. Neurosurgery. 53:899-905; discussion 905-906, 2003.
20.
Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC: Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery. 44:1005-1017, 1999.
EP
TE D
M AN U
SC
RI PT
13.
22.
23.
24.
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21. Morrissy RT, Goldsmith GS, Hall EC, Kehl D, Cowie GH: Measurement of the Cobb angle on radiographs of patients who have scoliosis. Evaluation of intrinsic error. J Bone Joint Surg Am. 72:320-327, 1990. Mottolese C, Szathmari A, Simon E, Rousselle C, Ricci-Franchi AC, Hermier M: Treatment of Chiari type I malformation in children: the experience of Lyon. Neurol Sci. 32 Suppl 3:S325-330, 2011.
Navarro R, Olavarria G, Seshadri R, Gonzales-Portillo G, McLone DG, Tomita T: Surgical results of posterior fossa decompression for patients with Chiari I malformation. Childs Nerv Syst. 20:349-356, 2004. Oldfield EH, Muraszko K, Shawker TH, Patronas NJ: Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg. 80:3-15, 1994. 10
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25. Ono A, Ueyama K, Okada A, Echigoya N, Yokoyama T, Harata S: Adult scoliosis in syringomyelia associated with Chiari I malformation. Spine. 27:E23-28, 2002. Rocque BG, George TM, Kestle J, Iskandar BJ: Treatment practices for Chiari malformation type I with syringomyelia: results of a survey of the American Society of Pediatric Neurosurgeons. J Neurosurg Pediatr. 8:430-437, 2011.
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26.
27. Sahuquillo J, Rubio E, Poca MA, Rovira A, Rodriguez-Baeza A, Cervera C: 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. 35:874-884; discussion 884-885, 1994.
29.
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28. Silva JA, Melo LR, Araujo AF, Santos JAA: Resolution of syringomyelia in ten cases of "up-and-down Chiari malformation" after posterior fossa decompression. Arquivos de neuro-psiquiatria. 68:694-699, 2010. Tisell M, Wallskog J, Linde M: Long-term outcome after surgery for Chiari I malformation. Acta Neurol Scand. 120:295-299, 2009.
30. Tubbs RS, Iskandar BJ, Bartolucci AA, Oakes WJ: A critical analysis of the Chiari 1.5 malformation. J Neurosurg. 101:179-183, 2004. Urbizu A, Poca MA, Vidal X, Rovira A, Sahuquillo J, Macaya A: MRI-based morphometric analysis of posterior cranial fossa in the diagnosis of chiari malformation type I. J Neuroimaging. 24:250-256, 2014.
32.
Yilmaz A, Kanat A, Musluman AM, Colak I, Terzi Y, Kayaci S, Aydin Y: When is duraplasty required in the surgical treatment of Chiari malformation type I based on tonsillar descending grading scale. World Neurosurg. 75:307-313, 2011.
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Figure Legends Fig. 1. The preoperative sagittal T2 weighted images show Chiari malformation type I of CTD grade I (A), grade II (B) and grade III (C). Their follow-up MR images at 6 months
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after SPFD show reconstruction of cistern magna, disappearance of syringomyelia and
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upward shift of the tonsils.
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Fig. 2. Cervical sagittal T2 weighted images of a patient with brainstem herniation (CM 1.5): preoperative images reveal tonsillar herniation, brainstem herniation and a syrinx extending from medulla oblongata to thoracic region (A); follow-up images at 6 months
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after SPFD show reconstruction of cistern magna but no obvious reduction of syrinx (B).
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Fig. 3. Images of a patient on whom intraoperative ultrasound was performed: preoperative
sagittal
T1
weighted
images
reveal
tonsillar
herniation
and
a
cervicothoracic syrinx (A); follow-up sagittal T1 weighted images at 6 months after SPFD show reconstruction of cistern magna and reduction of syrinx (B); intraoperative
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ultrasound images before dura mater incision show disappearance of the subarachnoid space (C); intraoperative ultrasound image after duraplasty demonstrate enlargement of
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the subarachnoid space (D).
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Table 1: Main manifestations and clinical outcomes during follow-up period Total number / Number of patients with syringomyelia
Number of improved patients (%)
Number of not improved patients (%)
Motor dysfunction
39 / 33
25 (64.1%)
14 (35.9%) (including 3 deteriorated)
Numbness
43 / 41
38 (88.4%)
Deficits of pain and temperature sensation
16 /16 13 / 6
Extremity /trunk pain
10 / 10
Other disorders
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Head /Neck pain
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Sensory disturbance
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Main clinical manifestations
5 (11.6%) (including 2 deteriorated)
14 (87.5%)
2 (10.5%)
12 (92.3%)
1 (7.7%)
9 (90.0%)
1 (14.3%)
3/1
3 (100%)
0 (0%)
Tinnitus
9/2
7 (77.8%)
2 (22.2%)
Hoarseness /Cough / Dysphagia
10 / 2
10 (100%)
0 (0%)
6/1
5 (83.3%)
1 (16.7%)
3/0
3 (100%)
0 (0%)
152 / 112
126 (82.9%)
26 (17.1%) (including 5 deteriorated)
Total
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Nausea /Vomiting
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Ataxia
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Diplopia
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Table 2: Main disorders associated with CMI
36.8%
Brainstem herniation
38
25.0%
Ventricular dilation
21
13.8%
Basilar invagination
17
11.2%
Assimilation of the atlas
7
4.6%
Klippel-Feil syndrome
5
3.3%
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56
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Scoliosis
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Number of patients Percentage
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Disorder
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Highlights： ：
The efficacy of small-bone-window posterior fossa decompression (SPFD) with duraplasty for Chiari malformation type I (CMI) is controversial and the risk factors of clinical outcome remain unclear. We aim to provide clinical evidence. All the patients underwent combined surgical procedures: a small-bone-window sub-
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occipital decompression (diameter, 2.5-3cm) and a C1 laminectomy (1.5-2cm wide) followed by a duraplasty with an autologous graft.
Long-term follow-up was performed with a average duration of 74 months.
Relevant index indicating the poor clinical outcome were analyzed.
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Abbreviations list： ： CM: Chiari malformation CMI: Chiari malformation type I
CTD: cerebellar tonsil descent MR: magnetic resonance SM: syringomyelia
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SPFD: small-bone-window posterior fossa decompression
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CSF: cerebrospinal fluid
S1878-8750(15)00083-2
DOI:
10.1016/j.wneu.2015.02.006
Reference:
WNEU 2715
To appear in:
World Neurosurgery
Received Date: 6 October 2014 Revised Date:
1 February 2015
Accepted Date: 4 February 2015
Please cite this article as: Deng X, Yang C, Gan J, Wu L, Yang T, Yang J, Xu Y, Long-term outcomes following small-bone-window posterior fossa decompression and duraplasty in adults with Chiari malformation type I, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.02.006. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1 Abstract Background:
Small-bone-window
posterior
fossa
decompression
(SPFD)
with
duraplasty is one of the popular surgical options for Chiari malformation type I (CMI), but
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its efficacy is controversial and the risk factors of clinical outcome remain unclear. Methods: The study cohort included 152 CMI patients who received SPFD at Beijing Tiantan hospital from January 2008 to September 2009. All the patients underwent combined surgical procedures: a small-bone-window sub-occipital decompression (diameter, 2.5-3cm) and a C1 laminectomy (1.5-2cm wide) followed by a duraplasty with
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an autologous graft. Clinical manifestations, radiological features and follow-up data over a six-year span were analyzed. Risk factors associated with outcome were investigated
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using chi-square analysis and logistic regression analysis.
Results: The average follow-up duration was 74 months. Symptoms were improved in 126 patients (82.9%), remained stable in 21 patients (13.8%), and deteriorated in 5 patients (3.3%). There was no mortality. Postoperative magnetic resonance (MR) images were available in all patients. Preoperatively 112 patients were associated with syringomyelia (SM), and the follow-up MR images showed obvious reduction of SM in 73 patients (65.2%) and no significant change in 39 patients (34.8%). Additionally, cistern
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magna enlargement was observed in 92 patients (85.2%). Regression analysis indicates preoperative motor dysfunction, brainstem herniation and basilar invagination may influence the clinical outcome (p<0.05).
Conclusions: Small-bone-window posterior fossa decompression with duraplasty is an
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effective and safe treatment option with a low complication rate. Motor dysfunction,
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brainstem herniation and basilar invagination are predictors of poor clinical prognosis.
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Title Page Long-term outcomes following small-bone-window posterior fossa
Xiaofeng Deng *, a, M.D. Chenlong Yang *, a, M.D.
Liang Wu a, M.D.
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Tao Yang a, M.D.
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Jiahe Gan b, M.D.
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decompression and duraplasty in adults with Chiari malformation type I
Jun Yang a, M.D.
Yulun Xu a, M.D., Ph.D.
* Xiaofeng Deng and Chenlong Yang contributed to the work equally and should be
a
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regarded as co-first authors.
Department of Neurosurgery, China National Clinical Research Center for Neurological
Diseases, Beijing Tiantan Hospital, Capital Medical University, No. 6 Tiantan Xili, Dongcheng District, Beijing 100050, China.
School of Clinical Medicine, Capital Medical University, No. 10 Xitoutiao, Youanmen,
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b
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Fengtai District, Beijing 100069, China.
Correspondence to: Prof. Yulun Xu, M.D., Ph.D. Tel: +86-13501285331, fax: +86-10-6709-6523; E-mail: [email protected]
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Introduction Chiari malformation (CM), also known as Arnold-Chiari malformation, is a congenital malformation characterized by a downward displacement of the cerebellar tonsils into the spinal canal (9, 22). CM can be divided into four types, in which Chiari malformation
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type I (CMI) is the most common. The mechanism of CM remains unclear, and the majority of scholars support the view that it is resulting from the reduced capacity of the posterior cranial fossa, which has been demonstrated by studies on the morphology of posterior cranial fossa (4, 9, 20). CM may be complicated by a variety of other
invagination, occipitalization and scoliosis (8).
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malformations, including syringomyelia (SM), hydrocephalus, platybasia, basilar
Regarding the treatment of CMI, most authors agree that posterior fossa
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decompression can lead to both clinical and radiological improvement (10, 13, 23, 2729). However, specific surgical procedures remain controversial, such as craniectomy and bone-window size, whether the arachnoid should be opened and whether cerebellar tonsil should be manipulated (13, 19, 26, 27, 32). Besides, the risk factors on prognosis are still ambiguous.
The current study aims to evaluate the efficacy of small-bone-window posterior fossa decompression (SPFD) with duraplasty in the treatment of CMI, and to analyze the
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related predictors of poor outcome. Materials and methods
The study was approved by the Institutional Review Board and Ethics Committee of
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Beijing Tiantan Hospital, Capital Medical University. The cohort included 152 CMI patients who received SPFD in our department from January 2008 to September 2009.
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Exclusion criteria included (a) occipitocervical instability; or (b) incomplete data. Clinical presentations
Clinical symptoms and physical examinations were recorded, including headache, sensory-motor disturbance, and muscle atrophy. The main clinical manifestations were classified into five groups: 1) sensory disturbance, including numbness, and deficits of pain and temperature sensation, 2) motor dysfunction, including weakness of limbs and muscle atrophy, 3) head and/or neck pain, 4) extremity and/or trunk pain, 5) other neurological disorders, including diplopia, tinnitus, hoarseness, cough, dysphagia, ataxia, and nausea or vomiting.
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Imaging Preoperative magnetic resonance (MR) imaging of the cervical spine was performed on all patients. The descending distance between the inferior pole of the cerebellar tonsil and level of the foramen magnum was measured on sagittal T1-weighted images. The
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degree of cerebellar descent was classified into three groups based on the cerebellar tonsil descent (CTD) grading scale: 1) Grade I, the tonsil descends over the foramen magnum but does not reach the C1 arch; 2) Grade II, the tonsil descends to C1 arch level; 3) Grade III, the tonsil descends below the C1 arch.
The location of SM was determined in sagittal MR images and it was classified
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into cervical, cervicothoracic and holocord syrinx. Other associated abnormalities were also recorded, such as ventricular dilation, scoliosis, basilar invagination, occipitalization
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and Klippel-Feil syndrome. Ventricular dilation was defined as Evans’ index >0.30 (3) and scoliosis was defined as the curve angle ≥10º according to the Cobb method (7, 11, 21, 25). Surgical approach
Small-bone-window posterior fossa decompression with duraplasty was performed on all patients. After patients were left-lateral positioned, a posterior midline skin incision was
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made from 1cm below the inion to the spinous process of C4 and an autologous graft (2cm×2cm) was resected from the fascia and reserved. A SPFD procedure including a small-bone-window
sub-occipital
craniectomy
(diameter,
2.5-3cm)
and
a
C-1
laminectomy (1.5-2cm) was performed. The thick and constraining dural band found at
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the occipital-cervical junction was resected. The dura mater was opened with the arachnoid intact, and then the dura mater was grafted with the autologous graft to enlarge the cistern magna.
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Besides, 28 patients in the cohort underwent intraoperative ultrasound examinations. The volume of subarachnoid space around the tonsils was measured both before dura mater incision and after grafting. Doppler ultrasound diagnostic system (GE Logiq 5) was used (5~8 MHz, probe size 8mmx15 mm). Prior to dura mater incision, the bone window was filled with sterilizing saline, and epidural detection was performed putting the probe close to the dura mater. Ultrasonography showed disappearance of the cisterna magna (Fig. 3c). After duraplasty with autologous fascia, epidural detection was repeated. The enlargement of the subarachnoid space (≥ 3mm) and the reconstruction of cisterna magna could confirm the efficiency of decompression (Fig. 3d).
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Follow-up Follow-up data for all patients were obtained during individual office visits or telephone interviews. MR imaging was performed postoperatively, at discharge, and semi-annually or annually thereafter. The clinical outcomes were categorized as follows: 1) Improved:
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the patients experienced a partial or complete relief of their symptoms or neurological examination showed observable improvement. 2) Not improved: Slight or no change in symptoms, or worsening of their clinical status. The clinical symptoms and neurological functions were assessed independently by two neurosurgeons, reviewed and processed
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by another evaluator. Statistical evaluation
SPSS 18.0 software (SPSS Inc., Chicago, IL, USA) was used for statistical analyses.
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Chi-square test was used to screen the potential risk factors, including gender, age at onset, age at diagnosis, duration of symptoms, main clinical presentations, CTD grades, syringomyelia, hydrocephalus, brainstem herniation, basilar invagination, and scoliosis. Furthermore, logistic analysis was performed to identify the risk factors on prognosis. Probability (p) values ≤0.05 were considered significant. Results
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Patient population and clinical characteristics From January 2008 through September 2009, 158 consecutive CMI patients underwent SPFD in our department. Six patients were lost to follow-up and excluded; a total of 152 patients were enrolled in the study. There were 52 males and 100 females, with a male-
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to-female ratio of 1:1.92. The average age at time of surgery was 39.2 ±11.7 years (range 18 to 60 years). Ages at onset ranged from 7 to 58 years (mean 33.1 ±11.2
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years). The duration of symptoms ranged from 1 to 420 months (mean 66 months; median 36 months). According to the main clinical-manifestation categorization, 39 patients had motor dysfunction, 59 patients had sensory disturbance, 13 patients had head and/or neck pain, 10 patients had extremity and/or trunk pain, and 31 patients had other neurological disorders. The main clinical manifestations were summarized in table 1. Preoperative imaging The distance of tonsillar herniation ranged from 5.0 to 27.0 mm (mean 9.4 ±4.8mm). According to the CTD grading criteria, 72 patients (47.4%) were identified with Grade I 4
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(Fig. 1a), 53 patients (34.9%) with Grade II (Fig. 1b), and 27 patients (17.7%) with Grade III (Fig. 1c). Concomitant SM was observed in 112 patients (73.7%): 18 (16.1%) with a cervical syrinx, 86 (76.8%) with a cervicothoracic syrinx and 8 (7.1%) with a holocord
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syrinx. The other disorders associated with CMI were summarized in Table 2. Complications and follow-up
Meningitis occurred in seven patients after operation, and all were effectively controlled by antibiotics and lumbar drainage. One patient developed cerebrospinal fluid (CSF) leak, which was resolved following conservative treatment. There was no mortality in this
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cohort. Follow-up data for all patients were available, with a mean duration of 74 months. Symptoms were improved in 126 patients (82.9%), remained unchanged in 21 patients (13.8%), and deteriorated in 5 patients (3.3%). Patients with motor dysfunction showed a
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significantly lower improvement rate (64.1%) than the other groups. The clinical outcomes during follow-up period were summarized in Table 1. Moreover, with regard to the preoperative MR features, patients with brainstem herniation showed a lower improvement rate (68.4%) than those without brainstem herniation (87.7%), and patients with basilar invagination also showed a lower improvement rate (58.8%) than patients without basilar invagination (85.9%).
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On admission, 112 patients were observed with concomitant SM. According to the follow-up MR images, SM disappeared or obviously reduced in 73 patients (65.2%, Fig. 1), and remained stable in the other 39 patients (34.8%). Cistern magna enlargement was observed in 92 patients (85.2%, Fig. 1a, d).
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Logistic analysis indicates motor dysfunction (p=0.006; OR=3.723; 95% CI, 1.467-9.452), brainstem herniation (p=0.026; OR=2.930; 95% CI, 1.135-7.562) and basilar invagination (p=0.038; OR=3.480; 95% CI, 1.071-11.311) had significant effects
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on poor clinical outcomes. Discussion
A popular hypothesis concerning the pathogenesis of CMI is that the hindbrain tissues are dislocated into the spinal canal due to an overcrowded posterior cranial fossa which is caused by the underdevelopment of the mesodermal occipital somite (9, 31). Concerning the formation of SM associated with CMI, there are several different hypotheses. While most of the authors agree the partial obstruction in the foramen magnum area, which blocks the normal circulation of CSF, is the pacing factor in the development of SM (16, 24). Thus, the optimal treatment for CMI should be enlarging 5
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the posterior cranial fossa and relieving the obstruction of CSF flow at the level of foramen magnum. Overall, SPFD can be an effective approach to treat CMI and SM. Surgical procedures of SPFD
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The size of bone window for posterior fossa decompression is under debate (1, 18). A large-bone-window posterior fossa decompression is effective to enlarge the posterior cranial fossa and to relieve the symptoms. However, there might be a higher incidence of complications, such as CSF leak, pseudo cyst, meningitis, and hydrocephalus (5). Besides, excessive removal of the squamous part of the occipital bone could lead to the
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downward and backward displacement of the cerebellum and brainstem, resulting in pseudocephalocele (cerebellum encephalocele from the bone window); thereby further
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obstructing the CSF flow and pulling the trigeminal, abducent, acoustic nerves and lower cranial nerves, leading to a succession of long-term complications. Furthermore, according to the previous studies (5, 6, 9, 15), a small-bone-window craniectomy is sufficient to achieve favorable clinical outcomes and the incidence of complications is obviously reduced. This procedure can not only relieve the compression of the occipitocervical bones, but can also preserve enough bones to support the cerebellum and brainstem. In the current study, all patients underwent a small-bone-window
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approach and high rates of clinical (82.9%) and radiological (85.2%) improvement were achieved. In the long-term follow-up period, no patient developed cerebellar ptosis or hydrocephalus.
Whether it is necessary to open the arachnoid space is another point of
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contention. Some authors believe that CSF-related complications, such as CSF leak and meningitis, are directly associated with the opening of arachnoid (23). The other authors indicate that the incidence of CSF leak does not increase in the arachnoid opening
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group as long as watertight duraplasty is performed, and reconstruction of the cistern magna and tonsillar manipulation could contribute to a better prognosis (2). In our experience, arachnoid opening was not necessary for most patients. SPFD and duraplasty without arachnoid incision is sufficient to relieve the compression and to improve clinical symptoms, and the incidence of CSF-related complications is low in our cohort. Besides, intraoperative ultrasound can be used to verify a satisfactory decompression manifested by increased subarachnoid space around the tonsils and tonsillar pulsation. In the present study, 28 patients underwent intraoperative ultrasound and all of them showed cistern magna enlargement (Fig. 3c, d), which demonstrates a 6
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SPFD and duraplasty without arachnoid incision can effectively relieve the compression at the level of the foramen magnum. Some authors point out that patients receiving herniated tonsil excision experienced better outcomes than patients without tonsillar manipulation, and thus
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attempts should be made to remove the herniated tonsils (5). However, the clinical and radiological results in our study were similar to the reported prognosis of other series in which tonsillar manipulation was performed (2, 5). Additionally, we found the herniated tonsil could shift upward after SPFD with duraplasty in most cases (85.2%) even if it was not manipulated (Fig. 1a, d), and the previous study had also demonstrated that the
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cerebellar tonsils and brainstem could undergo a gradual recovery to normalcy after decompression without tonsillar coagulation in most patients (12). This might result from
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the morphological plasticity of the brain tissues. The tonsillar herniation is generated by the overcrowding of the posterior cranial fossa, and after the capacity of the posterior cranial fossa is enlarged following SPFD, the herniated tonsils could move upward and return to the posterior cranial fossa. It may be unnecessary to manipulate the herniated tonsils for most CMI patients (Chiari malformation type 1.5 might be exceptions). Risk factors on prognosis
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The risk factors on prognosis are still in its infancy. Some authors indicate that ages at time of surgery and symptom duration are significantly associated with prognosis (2). And some studies also consider that age of onset is of vital importance (23). In the current study, a large cohort of 152 patients was enrolled and multivariate analysis was
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performed focusing on ten different factors. Regression analysis showed that the crucial clinical predictors of poor outcome were motor dysfunction, brainstem herniation and basilar invagination.
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According to the main manifestation categories, patients with motor dysfunction
revealed a lower recovery rate than the others, suggesting the impairment of the motor system was difficult to restore. Neurosurgeons may consider that patients whose chief complaints are muscle weakness and muscle atrophy may not respond well to decompression.
CMI along with brainstem herniation is also referred to Chiari malformation type 1.5 (CM 1.5) (14, 30). It is reported that there is no specific sign or symptom peculiar to CM 1.5, but the incidence of unresolved SM after SPFD is nearly two-fold higher in CM 1.5 than CMI. For CM 1.5 patients, a routine SPFD may not be sufficient to decompress
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the cerebella and brainstem, and a more aggressive surgical strategy might be needed to alleviate SM, including bone-window enlargement, arachnoid incision, manipulation of arachnoid adhesions and tonsillectomy. This study demonstrated that it was more difficult to relieve the symptoms and to reduce the syrinx size (Fig. 2) for CM 1.5 patients
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compared with CMI patients. The optimal procedure for CM 1.5 still needs further research.
Basilar invagination was also significantly associated with poor outcomes. For patients with basilar invagination, a pure SPFD may not be enough to relieve the compression on brainstem and cerebellum, especially the ventral compression from the
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odontoid tip. As some authors suggested in the literature, a ventral cervicomedullary junction decompression could be attempted in these cases (17).
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Limitations
For ethical and security considerations, there is no control group with large-bone-window posterior fossa decompression, or control group with arachnoid opening in this study. Conclusions
Small-bone-window posterior fossa decompression with duraplasty is an effective and safe treatment option with a low complication rate. Motor dysfunction, brainstem
Acknowledgments
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herniation and basilar invagination are predictors of poor clinical prognosis.
We thank all of the patients who trusted us with their care, and all of the physicians and
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staff who helped in this study. Conflict of interest
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The authors have no conflicts of interest to disclose.
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References
Abd-El-Barr M, Groff MW: Less is more: limiting the size of posterior fossa decompressions in Chiari I malformations. World Neurosurg. 81:706-707, 2014.
2.
Alfieri A, Pinna G: Long-term results after posterior fossa decompression in syringomyelia with adult Chiari Type I malformation. J Neurosurg Spine. 17:381387, 2012.
3.
Ambarki K, Israelsson H, Wahlin A, Birgander R, Eklund A, Malm J: Brain ventricular size in healthy elderly: comparison between Evans index and volume measurement. Neurosurgery. 67:94-99; discussion 99, 2010.
SC
RI PT
1.
M AN U
4. Aydin S, Hanimoglu H, Tanriverdi T, Yentur E, Kaynar MY: Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surg Neurol. 64:237-241; discussion 241, 2005. Bao C, Yang F, Liu L, Wang B, Li D, Gu Y, Zhang S, Chen L: Surgical treatment of Chiari I malformation complicated with syringomyelia. Exp Ther Med. 5:333-337, 2013.
6.
Batzdorf U, McArthur DL, Bentson JR: Surgical treatment of Chiari malformation with and without syringomyelia: experience with 177 adult patients. J Neurosurg. 118:232-242, 2013.
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5.
EP
7. Brockmeyer D, Gollogly S, Smith JT: Scoliosis associated with Chiari 1 malformations: the effect of suboccipital decompression on scoliosis curve progression: a preliminary study. Spine. 28:2505-2509, 2003.
9.
10.
AC C
8. Colombo LF, Motta F: Consensus conference on Chiari: a malformation or an anomaly? Scoliosis and others orthopaedic deformities related to Chiari 1 malformation. Neurol Sci. 32 Suppl 3:S341-343, 2011. Dagtekin A, Avci E, Kara E, Uzmansel D, Dagtekin O, Koseoglu A, Talas D, Bagdatoglu C: Posterior cranial fossa morphometry in symptomatic adult Chiari I malformation patients: comparative clinical and anatomical study. Clin Neurol Neurosurg. 113:399-403, 2011. El-Ghandour NM: Long-term outcome of surgical management of adult Chiari I malformation. Neurosurg Rev. 35:537-546; discussion 546-547, 2012.
11. Eule JM, Erickson MA, O'Brien MF, Handler M: Chiari I malformation associated with syringomyelia and scoliosis: a twenty-year review of surgical and nonsurgical treatment in a pediatric population. Spine. 27:1451-1455, 2002.
9
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12. Heiss JD, Suffredini G, Bakhtian KD, Sarntinoranont M, Oldfield EH: Normalization of hindbrain morphology after decompression of Chiari malformation Type I. J Neurosurg. 117:942-946, 2012. Imperato A, Seneca V, Cioffi V, Colella G, Gangemi M: Treatment of Chiari malformation: who, when and how. Neurol Sci. 32 Suppl 3:S335-339, 2011.
14.
Kim IK, Wang KC, Kim IO, Cho BK: Chiari 1.5 malformation : an advanced form of Chiari I malformation. J Korean Neurosurg Soc. 48:375-379, 2010.
15.
Klekamp J: Surgical treatment of Chiari I malformation--analysis of intraoperative findings, complications, and outcome for 371 foramen magnum decompressions. Neurosurgery. 71:365-380; discussion 380, 2012.
16.
Koyanagi I, Houkin K: Pathogenesis of syringomyelia associated with Chiari type 1 malformation: review of evidences and proposal of a new hypothesis. Neurosurg Rev. 33:271-284; discussion 284-285, 2010.
17.
Menezes AH: Craniovertebral junction abnormalities with hindbrain herniation and syringomyelia: regression of syringomyelia after removal of ventral craniovertebral junction compression. J Neurosurg. 116:301-309, 2012.
18.
Menezes AH: Current opinions for treatment of symptomatic hindbrain herniation or Chiari type I malformation. World Neurosurg. 75:226-228, 2011.
19.
Milhorat TH, Bolognese PA: Tailored operative technique for Chiari type I malformation using intraoperative color Doppler ultrasonography. Neurosurgery. 53:899-905; discussion 905-906, 2003.
20.
Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC: Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery. 44:1005-1017, 1999.
EP
TE D
M AN U
SC
RI PT
13.
22.
23.
24.
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21. Morrissy RT, Goldsmith GS, Hall EC, Kehl D, Cowie GH: Measurement of the Cobb angle on radiographs of patients who have scoliosis. Evaluation of intrinsic error. J Bone Joint Surg Am. 72:320-327, 1990. Mottolese C, Szathmari A, Simon E, Rousselle C, Ricci-Franchi AC, Hermier M: Treatment of Chiari type I malformation in children: the experience of Lyon. Neurol Sci. 32 Suppl 3:S325-330, 2011.
Navarro R, Olavarria G, Seshadri R, Gonzales-Portillo G, McLone DG, Tomita T: Surgical results of posterior fossa decompression for patients with Chiari I malformation. Childs Nerv Syst. 20:349-356, 2004. Oldfield EH, Muraszko K, Shawker TH, Patronas NJ: Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg. 80:3-15, 1994. 10
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25. Ono A, Ueyama K, Okada A, Echigoya N, Yokoyama T, Harata S: Adult scoliosis in syringomyelia associated with Chiari I malformation. Spine. 27:E23-28, 2002. Rocque BG, George TM, Kestle J, Iskandar BJ: Treatment practices for Chiari malformation type I with syringomyelia: results of a survey of the American Society of Pediatric Neurosurgeons. J Neurosurg Pediatr. 8:430-437, 2011.
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26.
27. Sahuquillo J, Rubio E, Poca MA, Rovira A, Rodriguez-Baeza A, Cervera C: 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. 35:874-884; discussion 884-885, 1994.
29.
M AN U
SC
28. Silva JA, Melo LR, Araujo AF, Santos JAA: Resolution of syringomyelia in ten cases of "up-and-down Chiari malformation" after posterior fossa decompression. Arquivos de neuro-psiquiatria. 68:694-699, 2010. Tisell M, Wallskog J, Linde M: Long-term outcome after surgery for Chiari I malformation. Acta Neurol Scand. 120:295-299, 2009.
30. Tubbs RS, Iskandar BJ, Bartolucci AA, Oakes WJ: A critical analysis of the Chiari 1.5 malformation. J Neurosurg. 101:179-183, 2004. Urbizu A, Poca MA, Vidal X, Rovira A, Sahuquillo J, Macaya A: MRI-based morphometric analysis of posterior cranial fossa in the diagnosis of chiari malformation type I. J Neuroimaging. 24:250-256, 2014.
32.
Yilmaz A, Kanat A, Musluman AM, Colak I, Terzi Y, Kayaci S, Aydin Y: When is duraplasty required in the surgical treatment of Chiari malformation type I based on tonsillar descending grading scale. World Neurosurg. 75:307-313, 2011.
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Figure Legends Fig. 1. The preoperative sagittal T2 weighted images show Chiari malformation type I of CTD grade I (A), grade II (B) and grade III (C). Their follow-up MR images at 6 months
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after SPFD show reconstruction of cistern magna, disappearance of syringomyelia and
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upward shift of the tonsils.
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Fig. 2. Cervical sagittal T2 weighted images of a patient with brainstem herniation (CM 1.5): preoperative images reveal tonsillar herniation, brainstem herniation and a syrinx extending from medulla oblongata to thoracic region (A); follow-up images at 6 months
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after SPFD show reconstruction of cistern magna but no obvious reduction of syrinx (B).
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Fig. 3. Images of a patient on whom intraoperative ultrasound was performed: preoperative
sagittal
T1
weighted
images
reveal
tonsillar
herniation
and
a
cervicothoracic syrinx (A); follow-up sagittal T1 weighted images at 6 months after SPFD show reconstruction of cistern magna and reduction of syrinx (B); intraoperative
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ultrasound images before dura mater incision show disappearance of the subarachnoid space (C); intraoperative ultrasound image after duraplasty demonstrate enlargement of
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the subarachnoid space (D).
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Table 1: Main manifestations and clinical outcomes during follow-up period Total number / Number of patients with syringomyelia
Number of improved patients (%)
Number of not improved patients (%)
Motor dysfunction
39 / 33
25 (64.1%)
14 (35.9%) (including 3 deteriorated)
Numbness
43 / 41
38 (88.4%)
Deficits of pain and temperature sensation
16 /16 13 / 6
Extremity /trunk pain
10 / 10
Other disorders
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Head /Neck pain
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Sensory disturbance
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Main clinical manifestations
5 (11.6%) (including 2 deteriorated)
14 (87.5%)
2 (10.5%)
12 (92.3%)
1 (7.7%)
9 (90.0%)
1 (14.3%)
3/1
3 (100%)
0 (0%)
Tinnitus
9/2
7 (77.8%)
2 (22.2%)
Hoarseness /Cough / Dysphagia
10 / 2
10 (100%)
0 (0%)
6/1
5 (83.3%)
1 (16.7%)
3/0
3 (100%)
0 (0%)
152 / 112
126 (82.9%)
26 (17.1%) (including 5 deteriorated)
Total
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Nausea /Vomiting
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Ataxia
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Diplopia
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Table 2: Main disorders associated with CMI
36.8%
Brainstem herniation
38
25.0%
Ventricular dilation
21
13.8%
Basilar invagination
17
11.2%
Assimilation of the atlas
7
4.6%
Klippel-Feil syndrome
5
3.3%
SC
56
AC C
EP
TE D
Scoliosis
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Number of patients Percentage
M AN U
Disorder
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Highlights： ：
The efficacy of small-bone-window posterior fossa decompression (SPFD) with duraplasty for Chiari malformation type I (CMI) is controversial and the risk factors of clinical outcome remain unclear. We aim to provide clinical evidence. All the patients underwent combined surgical procedures: a small-bone-window sub-
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occipital decompression (diameter, 2.5-3cm) and a C1 laminectomy (1.5-2cm wide) followed by a duraplasty with an autologous graft.
Long-term follow-up was performed with a average duration of 74 months.
Relevant index indicating the poor clinical outcome were analyzed.
AC C
EP
TE D
M AN U
SC
ACCEPTED MANUSCRIPT
Abbreviations list： ： CM: Chiari malformation CMI: Chiari malformation type I
CTD: cerebellar tonsil descent MR: magnetic resonance SM: syringomyelia
AC C
EP
TE D
M AN U
SC
SPFD: small-bone-window posterior fossa decompression
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CSF: cerebrospinal fluid