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The case for duraplasty in adults undergoing posterior fossa decompression for Chiari I malformation: A systematic review and meta-analysis of observational studies
Clinical Neurology and Neurosurgery 125 (2014) 58–64
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
The case for duraplasty in adults undergoing posterior fossa decompression for Chiari I malformation: A systematic review and meta-analysis of observational studies Petter Förander a,∗ , Kristin Sjåvik b , Ole Solheim c,d , Ingrid Riphagen e , Sasha Gulati c,f , Øyvind Salvesen e , Asgeir Store Jakola c,d,g a
Department of Neurosurgery, Karolinska University Hospital, Stockholm, Sweden Department of Ophthalmology and Neurosurgery, University Hospital of Northern Norway, Tromsø, Norway c Department of Neurosurgery, St. Olavs University Hospital, Trondheim, Norway d National Centre for Ultrasound and Image Guided Therapy, Trondheim, Norway e Unit for Applied Clinical Research, Norwegian University of Science and Technology, Trondheim, Norway f Norwegian Centre of Competence in Deep Brain Stimulation for Movement Disorders, Trondheim, Norway g MI Lab, Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway b
a r t i c l e
i n f o
Article history: Received 10 June 2014 Received in revised form 1 July 2014 Accepted 13 July 2014 Available online 21 July 2014 Keywords: Adult Chiari Duraplasty Meta-analysis Review
a b s t r a c t Background: Posterior fossa decompression is carried out to improve passage of cerebrospinal fluid (CSF) in patients with symptomatic Chiari 1 malformations (CM1), but the extent and means of decompression remains controversial. Dural opening with subsequent duraplasty may contribute to clinical outcome, but may also increase complication risk. The aim of this systematic review and meta-analysis is to assess the effects of durotomy with subsequent duraplasty on clinical outcome in surgical treatment of adults with CM1. Data sources and study eligibility criteria: We systematically searched MEDLINE, Embase and CENTRAL, and screened references in relevant articles and in UpToDate. Publications with previously untreated adults (>15 years) with CM1 with or without associated syringomyelia, treated in the period 1990–2013 were eligible. Interventions: Posterior fossa decompression with duraplasty (PFDD group) was compared to posterior fossa decompression with bony decompression alone (PFD group). Results: The search retrieved 233 articles. After the review we included 12 articles, but only 4 articles included posterior fossa decompression with both techniques. Only 2 out of 12 studies were prospective. The odds ratio (OR) for reoperation was 0.15 (95% CI 0.05–0.49) in the PFDD group compared to PFD (p = 0.002). The OR of clinical failure at follow-up was 1.06 (95% CI 0.52–2.14) for PFDD compared to PFD (p = 0.88). There was also no difference in syringomyelia improvement between techniques (p = 0.60). The OR for CSF-related complications were 6.12 (95% CI 0.37–101.83) for PFDD compared to PFD (p = 0.21). Conclusion: This systematic review of observational studies reveals higher reoperation rates after bony decompression alone, but clinical improvement was not higher after primary decompression with duraplasty. There are so far no high-quality studies that offer guidance in the choice of decompressive technique in adult CM1 patients. We think that a randomized controlled trial on this topic is both needed and feasible. © 2014 Elsevier B.V. All rights reserved.
∗ Corresponding author. Tel.: +46 8 51770377. E-mail addresses: [email protected], [email protected] (P. Förander), [email protected] (K. Sjåvik), [email protected] (O. Solheim), [email protected] (I. Riphagen), [email protected] (S. Gulati), [email protected] (Ø. Salvesen), [email protected] (A.S. Jakola). http://dx.doi.org/10.1016/j.clineuro.2014.07.019 0303-8467/© 2014 Elsevier B.V. All rights reserved.
P. Förander et al. / Clinical Neurology and Neurosurgery 125 (2014) 58–64
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Contents 1. 2.
3.
4. 5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Study selection criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Data search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Data extraction and management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1. Primary end-point effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2. Primary end-point safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.3. Secondary end-point effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.4. Secondary end-point safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Statistics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.1. Assessment of heterogeneity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.2. Sensitivity analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Effectiveness of intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Cerebrospinal fluid related complications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Author role . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Chari I malformation (CM1) is usually defined radiologically as herniation of the cerebellar tonsils below the foramen magnum caused by overcrowding of the posterior fossa. Typical symptoms consist of head and neck pain that often are worsened by rapid increase in abdominal pressure (i.e. Vasalva maneuver). CM1 is associated with syringomyelia in approximately two thirds of patients [20]. The exact mechanisms behind CM1 and the frequently associated syringomyelia are still incompletely understood and a matter of debate [2,3,5,20]. Today, the diagnosis of both CM1 and syringomyelia is most often established by magnetic resonance imaging (MRI) [20]. MRI techniques can also be used to study cerebrospinal fluid (CSF) flow dynamics [27], while computed tomography (CT) can be useful to study bone anomalies in the craniocervical junction. For patients with symptomatic CM1 the mainstay of treatment is surgical decompression with the aim of improving passage of CSF in the foramen magnum region. The extent of decompression necessary to achieve this remains controversial as some argue for posterior fossa decompression removing only bone, while others claim that the opening of dura (with or without additional intradural procedures) is necessary for favorable clinical outcome [3,5,13,17,22,31]. However, opening of the dura is also associated with the risk of CSFrelated complications (e.g. prolonged hospital stay, CSF-leakage in need of additional intervention and risk of CNS infection) [9,11]. A majority of clinical studies on the treatment of CM1consists of surgical series or intervention studies with limited statistical power. A systematic review preferably with a meta-analysis is better equipped to illuminate this area of diverging surgical practice and might contribute to an answer where clinical practice is uncertain. Two recent systematic reviews in the pediatric population concluded that durotomy with subsequent duraplasty is associated with a lower risk of reoperation due to absence of clinical improvement, but with a greater risk for CSF-related complications [9,11]. Adults may differ significantly in this regard since they present with symptoms at a later stage with perhaps less compromised CSF circulation. On the other hand, the adult dura may be less distensible and bony decompression alone may therefore offer inadequate expansion. The problem with CSF leakage may also be more pronounced in children with less muscle and subcutaneous tissue
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coverage. These potentially clinical important differences justify a separate review in the adult population. The aim of this systematic review and meta-analysis is to assess clinical outcomes after posterior fossa decompression with additional durotomy with subsequent duraplasty compared to posterior fossa decompression alone in adults with CM1. 2. Methods 2.1. Study selection criteria In accordance with the PRISMA guidelines [21], we designed a systematic review and meta-analysis protocol (PROSPERO 2013:CRD42013006252) to analyze previously untreated adult (>15 years) patients with CM1 with or without associated syringomyelia, but without tethering or myelomeningocele. Clinical studies reporting on patients treated in the period 1990–2013 were eligible for inclusion. The interventions compared were posterior fossa decompression with duraplasty (PFDD) and posterior fossa decompression with bony decompression alone (PFD). Studies to be included were randomized controlled trials (RCTs) or quasi-RCTs (S1), but also observational studies (S2) including cohort studies, case–control studies or case series with ≥20 patients. This was decided as few or no S1 studies were expected, and S2 studies could supplement the evidence. Also, in the case of only low-quality evidence this strategy would effectively elucidate the need of performing better studies [12]. Further, we decided that the main meta-analysis should be performed with the S1 group while a supplementary analysis should be performed using the S2 cohort as long as the heterogeneity between studies remained acceptable (i.e. not approaching 100%). Also, detailed exclusion criteria are presented in the supplementary material. After the review of the literature it was apparent that no studies fulfilled criteria for S1 and therefore this systematic review consists only of S2-studies. 2.2. Data search A librarian (IIR) performed the searches in Embase, PubMed (includes MEDLINE), Cochrane Central Register of Controlled Trials (CENTRAL) and ClinicalTrials.gov. UpToDate was also screened for relevant articles.
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Only articles written or translated into English were included in this systematic review. The searches were run in the period September, 5–9 2013. The search details are presented in the supplementary material. Furthermore, reference lists of the reviewed articles were screened for additional relevant papers by the two investigators performing the review (ASJ, PF).
2.4.2. Sensitivity analysis If eligibility for some of the studies in the meta-analysis was questionable due to important sources of bias or lack of details, sensitivity analysis was planned by performing the meta-analysis both with and without these studies. 3. Results
2.3. Data extraction and management Data was extracted from included studies independently by two investigators (PF and ASJ) using a standardized data collection form. Cases of disagreement were solved by discussion, also including a third independent reviewer (OS). All variables in the data collection form are presented in the supplementary material. In case of overlapping or similar patient cohort reported in more than one publication the publication most suitable for this systematic review was included. In studies where other entities than CM1 were included (e.g. Chiari II or achondroplasia) and where the patient population consisted of both pediatric and adult patients the authors were contacted by e-mail in an attempt to extract data concerning patients fulfilling inclusion criteria for this systematic review. If we did not receive a reply a reminder was sent. If the reminder remained unanswered the study was excluded. 2.3.1. Primary end-point effect Proportions of patients re-operated due to clinical failure in the two groups.
The selection process is described in detail in Fig. 1. We retrieved 233 articles, but after the review process only 12 articles were included [1,5,10,15,16,18,22,23,25,26,28,30]. However, only four articles included posterior fossa decompression with both techniques (i.e. PFD vs PFDD) [10,16,22,30]. Thus, 8 of 12 articles for the purpose of our research question were case-series without control groups. Also, only 2 out of 12 articles had a prospective design, both comparing different duraplasty materials [18,28]. The characteristics of included studies are presented in Table 1 and the outcomes from individual studies are presented in Table 2. For each end-point in both treatment arms we tested heterogeneity to decide whether we could perform a meta-analysis of the observational studies. The heterogeneity was found to be less than 90% for all end-points. For details concerning heterogeneity see supplementary material. Based on the assumption that data from individual studies were similar enough to be grouped for the purpose of meta-analyses we merged all data into a PFDD group or PFD group. 3.1. Effectiveness of intervention
2.3.2. Primary end-point safety Proportions of patients with CSF related complications in the two groups. 2.3.3. Secondary end-point effect Proportions of clinical improvement (as defined by the researchers). Proportions of syringomyelia improvement as assessed by MRI. 2.3.4. Secondary end-point safety Proportions of re-operations due to CSF related complications. 2.4. Statistics We based our study on the Cochrane Handbook for Systematic Reviews of Interventions (edition 5.1.0. updated March 2011, www.cochrane-handbook.org). The review was prepared using RevManager version 5.1 (Cochrane Reviews) and I2 -statistics of observational studies were carried out with SPSS (version 18.0). Because only S2-studies were retrieved a random effect model was chosen because baseline, follow-up and outcome reporting were presumably different between studies. End-points were dichotomous and are presented as frequencies and odds ratio (OR) with 95% confidence interval (CI). 2.4.1. Assessment of heterogeneity Heterogeneity was assessed for each end-point in both treatment arms and tested by I2 which measured inconsistency (percentage of total variation across studies resulting from heterogeneity) of effects. In the event of >50% heterogeneity, we planned to use a random effect as described in the Cochrane Handbook for Systematic Reviews of Interventions. If severe heterogeneity (approximating 100%) was present for any end-point in either treatment group a meta-analysis would not be performed for that specific end-point.
Of the 432 surgeries in the PFDD group there were 8 (2%) re-operations due to clinical failure while there were 5 (11%) reoperations after the 46 in the PFD group. This is presented in Fig. 2. Lack of marked clinical improvement (as defined by researchers) was seen in 96 (23%) of 426 surgeries in the PFDD group. In the PFD group 11 (22%) of 51 had lack of improvement at the end of follow up, that is after the primary or secondary operations. This is presented in Fig. 3. In Fig. 4 we present the subgroup of patients with syringomyelia. In the PFDD group 65 (22%) of 298 surgeries did not lead to syringomyelia improvement assessed with postoperative MRI. In the PFD group 9 (26%) of 35 surgeries did not lead to syringomyelia improvement. 3.2. Cerebrospinal fluid related complications Figs. 5 and 6 summarize the CSF related complications between the treatments. In the PFDD group 32 (7%) of 472 surgeries lead to CSF related complication. In 18 (4%) of 438 surgeries invasive treatments were needed to repair the CSF leakage. None of the 41 patients in the PFD group had CSF related complications. 4. Discussion In this systematic review and meta-analysis of observational studies there were more re-operations due to lack of clinical improvement when PFD was performed compared to PFDD for CM1 in adults. However, at the end of follow up there were almost similar proportions of clinical improvement and syringomyelia improvement in both treatment groups. CSF related complications naturally occurred more frequent in the PFDD group, but the reviewed studies reported large variations in proportions of CSF related complications after PFDD. The difference in CSF-related complications between treatment groups was not statistically significant, but the low number of patients treated with PFD limits the statistical power of our meta-analysis.
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Fig. 1. Flow-chart of study inclusion.
Table 1 Characteristics of included studies. Authors
Year published
Duraplasty
Duraplasty type
No duraplasty
Prospective
Multi-center
Time to used follow-up (mo)
Mean age (y)
Aghakhani Batzdorf Erdogan Lam Lee Liu Munshi Sindou Spena Vanaclocha Williams Yilmaz SUM
2009 2013 2010 2013 2012 2005 2000 2002 2010 1997 2013 2011 –
151 26 15 22 20 40 14 44 36 26 34 58 486
Mix Mix Artificial Autologous Mix Mix Mix Autologous Unknown Mix Mix Mix –
0 0 12 0 5 0 10 0 0 0 0 24 51
No No No No No Yes No No No No Yes No 2/12
No No No No No No No No No No No No 0/12
88 89 NA 12 48 NA 6 12 40 6 3 9 –
38.3 NA 25.9 37.3 36.6 41.4 NA 40.0 40.4 28.5 38.7 38.9 –
Fig. 2. Re-operations due to clinical failure in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
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Table 2 Summary of results. Authors
PFDDa total
Re-opb
Failurec
Syrinxd
CSF relatede
CSF re-opf
PFDg total
Re-op
Failure
Syrinx
CSF related
CSF re-op
Aghakhani Batzdorf Erdogan Lam Lee Liu Munshi Sindou Spena Vanaclocha Williams Yilmaz
151 26 15 22 20 40 14 44 36 26 34 58
6/151 0/26 0/15 0/22 ?/20 0/40 0/14 0/44 2/36 0/26 ?/34 0/58
58/151 ?/26 4/15 1/22 0/20 6/40 3/14 8/44 7/36 3/26 ?/34 6/58
38/150 1/16 3/11 ?/? 6/20 ?/40 0/5 6/15 7/36 0/0 ?/? 4/45
7/151 0/26 3/15 1/22 0/20 0/40 ?/14 2/44 3/36 7/26 5/34 4/58
1/151 0/26 3/15 1/22 0/20 0/40 ?/14 1/44 3/36 7/26 ?/34 2/58
0 0 12 0 5 0 10 0 0 0 0 24
N/A N/A 1/12 0 ?/5 0 2/10 0 0 0 0 2/24
N/A N/A 2/12 N/A 1/5 N/A 3/10 N/A N/A N/A N/A 5/24
N/A N/A 0/4 N/A 2/5 N/A 4/7 N/A N/A N/A N/A 3/19
N/A N/A 0/12 N/A 0/5 N/A ?/10 N/A N/A N/A N/A 0/24
N/A N/A 0/12 N/A 0/5 N/A ?/10 N/A N/A N/A N/A 0/24
a b c d e f g
PFDD—group treated with posterior fossa decompression and duraplasty. Re-op—re-operated due to clinical failure. Failure—patients showing lack of improvement at end of follow-up. Syrinx—failure of syrinx regression assessed with postoperative MRI (independent of timing of assessment postoperatively). CSF related—complications possibly related to CSF (leakage, symptomatic pseudomeningocele, meningitis). CSF re-op—need of procedure to solve CSF related problems (e.g. lumbar drainage or re-operation). PFD—group treated with posterior fossa decompression alone without duraplasty.
Fig. 3. Patients failed to improve (as defined by the researchers) in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
Fig. 4. Failed to improve syringomyelia as assessed with postoperative MRI scan in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
Fig. 5. CSF related complications in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
Although this systematic review reveals higher reoperation rates in the PFD group, no apparent difference in lack of clinical improvement was seen between the two surgical techniques at the end of follow-up. However, more patients needed complementary surgery in the PFD group. Regardless of technique, a proportion of patients will remain symptomatic after posterior fossa decompression. Reasons may be wrong diagnosis, a chronic irreversible
pain conditions or medical or surgical complications leading to persistence of symptoms. If only PFD has been performed, reoperation with durotomy with subsequent duraplasty remains as an option. Thus, this unused treatment option may inflate the number of re-operations due to clinical failure in the PFD group. Where adequate PFDD was performed upfront and the patient fails to improve, no further surgical decompression can usually be
Fig. 6. Re-operations due to CSF related complications in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
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offered. Unfortunately, the included studies offer no insight into the success rates of re-operations with duroplasty after unsuccessful PFD. Although the difference in CSF complication rates between 7% and 0% after PFDD and PFD did not reach statistical significance, it is still likely that opening the meninges will increase CSF complication rates. From this systematic review we are unable to draw any conclusion on which technique that provides the best clinical outcome. Thus a staged approach in elective decompressive surgery for CM1 with PFD remains a feasible option, to minimize the risk of CSF complications. Using this approach a systematic and thorough follow-up is however required because some patients may require reoperations with duraplasty. Compared to the pediatric meta-analysis of decompressive surgery for CM1 the results in this meta-analysis on adult CM1 patients are fairly similar [9]. In the pediatric patients treated with PFDD 2.1% had re-operations compared to 12.6% in patients treated with PFD (2% and 11% in this meta-analysis, respectively). Although not statistically significant in the pediatric population more patients seemed to experience improvement (78.6% in PFDD vs 64.6% in PFD) and syringomyelia resolution (87% in PFDD vs 56.3% in PFD) after duraplasty. The proportions from our meta-analysis in adults were 77% in PFDD versus 78% in PFD for clinical improvement. Moreover, 78% treated with PFDD versus 74% treated with PFD experienced syringomyelia improvement as assessed with MRI. CSF related complications related to PFDD were seen in 19% of the pediatric surgeries compared to 7% after surgery in the adult population. Thus, it seems like both the effect of PFD and safety of PFDD is better in adult patients. The possibility remains that there is no universal strategy in decompressive surgery of CM1 patients. There may be useful tools for a tailored approach available, but further clinical validation is necessary. Electrophysiological studies have demonstrated that conduction time improvement in pediatric patients was most pronounced after bony decompression and division of the atlantooccipital membrane, with only slight or no additional improvement after duraplasty [4,32]. To what extent these indirect measures translate into clinical benefit remains unanswered, but these findings suggest that bony decompression alone may suffice in pediatric patients. Intraoperative ultrasound can be another tool of interest when attempting to tailor the approach [6,19]. Highfrequency probes clearly visualize the anatomy and when using color Doppler detailed flow-measurements are possible. In children it has been demonstrated that if CSF is pulsating behind the cerebellar tonsils after bony decompression further decompression with dural opening may not be necessary [29,31]. However, further systematic evaluation of the intraoperative findings encountered with electrophysiology and intraoperative ultrasound is needed before we can recommend using the techniques as routine guidance. After completed systematic search of literature and inclusion a recent study of 47 consecutive adults patients treated with PFD with long-term follow-up was published [14]. The mean followup was 111 months, longer than in all other included studies in the present review. The authors found long-term clinical improvement in approximately 60% of patients, and approximately 32% required reoperation with additional decompression. The first impression is that this failure rate seems high, but long-term improvement in the PFDD case series with longest follow-up (median 88 months) included in the present systematic review was 63% [1]. However, only 4% in that study underwent repeated decompression. The limitations of the existing literature represent the main limitation of this systematic review. There are no randomized studies or pseudo-randomized trials. The limited number of studies, the observational and retrospective character of most included studies, and the heterogeneity of studies must be taken into account when interpreting results from this systematic review. There were also few observational studies with bony decompression alone (PFD
63
group) that were eligible for inclusion. Also, 10 out of 12 included articles were retrospective with large variation in time to assessment between studies. In this case, the retrospective observational design and different follow up time of the included studies could affect proportions of clinical failure, but presumably the safety endpoints are less vulnerable in this regard. As eligibility for some of the studies in the meta-analysis was questionable due to important sources of bias or lack of details, sensitivity analysis was planned by performing the meta-analysis both with and without these studies. In the absence of high-quality studies, we decided against classifying the low-quality evidence further into more or less reliable. Assessment of publication bias was performed reporting proportion versus sample size in a funnel plot, but with only 12 studies included a reliable interpretation is difficult (see online material). Still, we did not find any clear indication of publication bias based on this assessment. According to the manual for systematic reviews, inclusion of observational studies is discouraged, due to the inherent risk of bias in these reports. Even with a sophisticated systematic review protocol, the results from the meta-analysis will not be more reliable than the data extracted from the individual studies (www.cochrane-handbook.org). This point to a general problem of systematic reviews and meta-analyses when high evidence studies are lacking, which is often the case in neurosurgery. We are not attempting scientific alchemy by drawing firm conclusions from uncontrolled observational data [7,8,24], but our review highlights the need of performing properly controlled studies on surgical techniques in CM1 patients. To reassure an indisputable endpoint in this heterogeneous material we used risk of reoperation as primary endpoint. However, there is reason to believe that reoperation is more likely to be recommended for patients with lack of improvement in the PFD group, compared to patients with clinical failure treated with PFDD, where fewer treatment options are available. In the end, the chance of clinical improvement was similar, but more patients in the PFD group needed a second operation to achieve this improvement.
5. Conclusion Although this systematic review of observational studies reveals higher reoperation rates with bony decompression alone, clinical improvement was not higher after primary decompression with duroplasty. Since the majority of patients will improve with PFD without duraplasty, a staged approach is still feasible to avoid CSF related complications. On the other hand the safety profile of PFDD in adults is better than in children, making this approach feasible if low complication rates can be documented. However, we encourage more systematic use of tools with subsequent systematic clinical assessments in an attempt to tailor the approach. At present there are no high-quality studies to offer guidance in the choice of decompressive technique in adult CM1 patients and we see no reasons why a RCT on surgical technique cannot be performed in non-emergent adult cases with CM1.
Author role Petter Förander: planning, revising protocol, data registration, analysis, interpretation, drafting article, submission of article. Kristin Sjåvik: publishing protocol (PROSPERO), interpretation, revising article. Ole Solheim: planning, revising protocol, data interpretation, revising article. Ingrid Riphagen: planning, revising protocol, systematic search and paper identification. Sasha Gulati: data interpretation, revising article.
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Øyvind Salvesen: planning, statistical supervision, revising article. Asgeir Store Jakola: planning, writing protocol, data registration, analysis and interpretation, drafting article, revising article, supervision. Protocol registration: PROSPERO 2013:CRD42013006252. Funding source None. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.clineuro. 2014.07.019. References [1] Aghakhani N, Parker F, David P, Morar S, Lacroix C, Benoudiba F, et al. Long-term follow-up of Chiari-related syringomyelia in adults: analysis of 157 surgically treated cases. Neurosurgery 2009;64:308–15. [2] Alden TD, Ojemann JG, Park TS. Surgical treatment of Chiari I malformation: indications and approaches. Neurosurg Focus 2001;11:E2. [3] Alfieri A, Pinna G. Long-term results after posterior fossa decompression in syringomyelia with adult Chiari Type I malformation. J Neurosurg Spine 2012;17:381–7. [4] Anderson RC, Emerson RG, Dowling KC, Feldstein NA. Improvement in brainstem auditory evoked potentials after suboccipital decompression in patients with Chiari I malformations. J Neurosurg 2003;98:459–64. [5] Batzdorf U, McArthur DL, Bentson JR. Surgical treatment of Chiari malformation with and without syringomyelia: experience with 177 adult patients. J Neurosurg 2013;118:232–42. [6] Cui LG, Jiang L, Zhang HB, Liu B, Wang JR, Jia JW, et al. Monitoring of cerebrospinal fluid flow by intraoperative ultrasound in patients with Chiari I malformation. Clin Neurol Neurosurg 2011;113:173–6. [7] De Witt Hamer PC, Gil Robles S, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a metaanalysis. J Clin Oncol 2012;30:2559–65. [8] Duffau H. The conceptual limitation to rely on intraoperative MRI in glioma surgery. World Neurosurg 2014 [Epub ahead of print]. [9] Durham SR, Fjeld-Olenec K. Comparison of posterior fossa decompression with and without duraplasty for the surgical treatment of Chiari malformation Type I in pediatric patients: a meta-analysis. J Neurosurg Pediatr 2008;2:42–9. [10] Erdogan E, Cansever T, Secer HI, Temiz C, Sirin S, Kabatas S, et al. The evaluation of surgical treatment options in the Chiari malformation type I. Turk Neurosurg 2010;20:303–13. [11] Hankinson T, Tubbs RS, Wellons J. Duraplasty or not? An evidence-based review of the pediatric Chiari I malformation. Child’s Nerv Syst 2011;27:35–40. [12] Ijaz S, Verbeek JH, Mischke C, Ruotsalainen J. Inclusion of nonrandomized studies in Cochrane systematic reviews was found to be in need of improvement. J Clin Epidemiol 2014;67:645–53. [13] Kalb S, Perez-Orribo L, Mahan M, Theodore N, Nakaji P, Bristol RE. Evaluation of operative procedures for symptomatic outcome after decompression surgery for Chiari type I malformation. J Clin Neurosci 2012;19:1268–72.
[14] Krishna V, McLawhorn M, Kosnik-Infinger L, Patel S. High long-term symptomatic recurrence rates after Chiari-1 decompression without dural opening: a single center experience. Clin Neurol Neurosurg 2014;118:53–8. [15] Lam FC, Penumaka A, Chen CC, Fischer EG, Kasper EM. Fibrin sealant augmentation with autologous pericranium for duraplasty after suboccipital decompression in Chiari 1 patients: a case series. Surg Neurol Int 2013;4. [16] Lee HS, Lee SH, Kim ES, Kim JS, Lee JI, Shin HJ, et al. Surgical results of arachnoid-preserving posterior fossa decompression for Chiari I malformation with associated syringomyelia. J Clin Neurosci 2012;19:557–60. [17] Limonadi FM, Selden NR. Dura-splitting decompression of the craniocervical junction: reduced operative time, hospital stay, and cost with equivalent early outcome. J Neurosurg 2004;101:184–8. [18] Liu B, Wang ZY, Li ZD, Ma CC, Sun JJ, Chen XD. Duraplasty with neuropatch versus autologous fascia lata for Chiari I malformation with syringomyelia: a comparative study. Beijing Da Xue Xue Bao 2005;37:629–32. [19] Milhorat TH, Bolognese PA. Tailored operative technique for Chiari type I malformation using intraoperative color Doppler ultrasonography. Neurosurgery 2003;53:899–905 (discussion 905-896). [20] Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, et al. Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 1999;44:1005–17. [21] Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009; 339. [22] Munshi I, Frim D, Stine-Reyes R, Weir BK, Hekmatpanah J, Brown F. Effects of posterior fossa decompression with and without duraplasty on Chiari malformation-associated hydromyelia. Neurosurgery 2000;46:1384–9 (discussion 1389-1390). [23] Sindou M, Chavez-Machuca J, Hashish H. Cranio-cervical decompression for Chiari type I-malformation, adding extreme lateral foramen magnum opening and expansile duroplasty with arachnoid preservation. Technique and long-term functional results in 44 consecutive adult cases—comparison with literature data. Acta Neurochir (Wien) 2002;144:1005–19. [24] Solheim O, Jakola AS, Unsgard G. Scientific alchemy and proposed gold standards of care. World Neurosurg 2014 [Epub ahead of print]. [25] Spena G, Bernucci C, Garbossa D, Valfre W, Versari P. Clinical and radiological outcome of craniocervical osteo-dural decompression for Chiari I-associated syringomyelia. Neurosurg Rev 2010;33:297–303. [26] Vanaclocha V, Saiz-Sapena N. Duraplasty with freeze-dried cadaveric dura versus occipital pericranium for Chiari type I malformation: comparative study. Acta Neurochir (Wien) 1997;139:112–9. [27] Ventureyra EC, Aziz HA, Vassilyadi M. The role of cine flow MRI in children with Chiari I malformation. Childs Nerv Syst 2003;19:109–13. [28] Williams LE, Vannemreddy PS, Watson KS, Slavin KV. The need in dural graft suturing in Chiari I malformation decompression: a prospective, single-blind, randomized trial comparing sutured and sutureless duraplasty materials. Surg Neurol Int 2013;4:26. [29] Yeh DD, Koch B, Crone KR. Intraoperative ultrasonography used to determine the extent of surgery necessary during posterior fossa decompression in children with Chiari malformation type I. J Neurosurg 2006;105:26–32. [30] Yilmaz A, Kanat A, Musluman AM, Colak I, Terzi Y, Kayaci S, et al. When is duraplasty required in the surgical treatment of Chiari malformation type I based on tonsillar descending grading scale? World Neurosurg 2011;75:307–13. [31] Yundt KD, Park TS, Tantuwaya VS, Kaufman BA. Posterior fossa decompression without duraplasty in infants and young children for treatment of Chiari malformation and achondroplasia. Pediatr Neurosurg 1996;25: 221–6. [32] Zamel K, Galloway G, Kosnik EJ, Raslan M, Adeli A. Intraoperative neurophysiologic monitoring in 80 patients with Chiari I malformation: role of duraplasty. J Clin Neurophysiol 2009;26:70–5.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
The case for duraplasty in adults undergoing posterior fossa decompression for Chiari I malformation: A systematic review and meta-analysis of observational studies Petter Förander a,∗ , Kristin Sjåvik b , Ole Solheim c,d , Ingrid Riphagen e , Sasha Gulati c,f , Øyvind Salvesen e , Asgeir Store Jakola c,d,g a
Department of Neurosurgery, Karolinska University Hospital, Stockholm, Sweden Department of Ophthalmology and Neurosurgery, University Hospital of Northern Norway, Tromsø, Norway c Department of Neurosurgery, St. Olavs University Hospital, Trondheim, Norway d National Centre for Ultrasound and Image Guided Therapy, Trondheim, Norway e Unit for Applied Clinical Research, Norwegian University of Science and Technology, Trondheim, Norway f Norwegian Centre of Competence in Deep Brain Stimulation for Movement Disorders, Trondheim, Norway g MI Lab, Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway b
a r t i c l e
i n f o
Article history: Received 10 June 2014 Received in revised form 1 July 2014 Accepted 13 July 2014 Available online 21 July 2014 Keywords: Adult Chiari Duraplasty Meta-analysis Review
a b s t r a c t Background: Posterior fossa decompression is carried out to improve passage of cerebrospinal fluid (CSF) in patients with symptomatic Chiari 1 malformations (CM1), but the extent and means of decompression remains controversial. Dural opening with subsequent duraplasty may contribute to clinical outcome, but may also increase complication risk. The aim of this systematic review and meta-analysis is to assess the effects of durotomy with subsequent duraplasty on clinical outcome in surgical treatment of adults with CM1. Data sources and study eligibility criteria: We systematically searched MEDLINE, Embase and CENTRAL, and screened references in relevant articles and in UpToDate. Publications with previously untreated adults (>15 years) with CM1 with or without associated syringomyelia, treated in the period 1990–2013 were eligible. Interventions: Posterior fossa decompression with duraplasty (PFDD group) was compared to posterior fossa decompression with bony decompression alone (PFD group). Results: The search retrieved 233 articles. After the review we included 12 articles, but only 4 articles included posterior fossa decompression with both techniques. Only 2 out of 12 studies were prospective. The odds ratio (OR) for reoperation was 0.15 (95% CI 0.05–0.49) in the PFDD group compared to PFD (p = 0.002). The OR of clinical failure at follow-up was 1.06 (95% CI 0.52–2.14) for PFDD compared to PFD (p = 0.88). There was also no difference in syringomyelia improvement between techniques (p = 0.60). The OR for CSF-related complications were 6.12 (95% CI 0.37–101.83) for PFDD compared to PFD (p = 0.21). Conclusion: This systematic review of observational studies reveals higher reoperation rates after bony decompression alone, but clinical improvement was not higher after primary decompression with duraplasty. There are so far no high-quality studies that offer guidance in the choice of decompressive technique in adult CM1 patients. We think that a randomized controlled trial on this topic is both needed and feasible. © 2014 Elsevier B.V. All rights reserved.
∗ Corresponding author. Tel.: +46 8 51770377. E-mail addresses: [email protected], [email protected] (P. Förander), [email protected] (K. Sjåvik), [email protected] (O. Solheim), [email protected] (I. Riphagen), [email protected] (S. Gulati), [email protected] (Ø. Salvesen), [email protected] (A.S. Jakola). http://dx.doi.org/10.1016/j.clineuro.2014.07.019 0303-8467/© 2014 Elsevier B.V. All rights reserved.
P. Förander et al. / Clinical Neurology and Neurosurgery 125 (2014) 58–64
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Contents 1. 2.
3.
4. 5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Study selection criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Data search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Data extraction and management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1. Primary end-point effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2. Primary end-point safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.3. Secondary end-point effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.4. Secondary end-point safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Statistics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.1. Assessment of heterogeneity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.2. Sensitivity analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Effectiveness of intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Cerebrospinal fluid related complications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Author role . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Chari I malformation (CM1) is usually defined radiologically as herniation of the cerebellar tonsils below the foramen magnum caused by overcrowding of the posterior fossa. Typical symptoms consist of head and neck pain that often are worsened by rapid increase in abdominal pressure (i.e. Vasalva maneuver). CM1 is associated with syringomyelia in approximately two thirds of patients [20]. The exact mechanisms behind CM1 and the frequently associated syringomyelia are still incompletely understood and a matter of debate [2,3,5,20]. Today, the diagnosis of both CM1 and syringomyelia is most often established by magnetic resonance imaging (MRI) [20]. MRI techniques can also be used to study cerebrospinal fluid (CSF) flow dynamics [27], while computed tomography (CT) can be useful to study bone anomalies in the craniocervical junction. For patients with symptomatic CM1 the mainstay of treatment is surgical decompression with the aim of improving passage of CSF in the foramen magnum region. The extent of decompression necessary to achieve this remains controversial as some argue for posterior fossa decompression removing only bone, while others claim that the opening of dura (with or without additional intradural procedures) is necessary for favorable clinical outcome [3,5,13,17,22,31]. However, opening of the dura is also associated with the risk of CSFrelated complications (e.g. prolonged hospital stay, CSF-leakage in need of additional intervention and risk of CNS infection) [9,11]. A majority of clinical studies on the treatment of CM1consists of surgical series or intervention studies with limited statistical power. A systematic review preferably with a meta-analysis is better equipped to illuminate this area of diverging surgical practice and might contribute to an answer where clinical practice is uncertain. Two recent systematic reviews in the pediatric population concluded that durotomy with subsequent duraplasty is associated with a lower risk of reoperation due to absence of clinical improvement, but with a greater risk for CSF-related complications [9,11]. Adults may differ significantly in this regard since they present with symptoms at a later stage with perhaps less compromised CSF circulation. On the other hand, the adult dura may be less distensible and bony decompression alone may therefore offer inadequate expansion. The problem with CSF leakage may also be more pronounced in children with less muscle and subcutaneous tissue
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coverage. These potentially clinical important differences justify a separate review in the adult population. The aim of this systematic review and meta-analysis is to assess clinical outcomes after posterior fossa decompression with additional durotomy with subsequent duraplasty compared to posterior fossa decompression alone in adults with CM1. 2. Methods 2.1. Study selection criteria In accordance with the PRISMA guidelines [21], we designed a systematic review and meta-analysis protocol (PROSPERO 2013:CRD42013006252) to analyze previously untreated adult (>15 years) patients with CM1 with or without associated syringomyelia, but without tethering or myelomeningocele. Clinical studies reporting on patients treated in the period 1990–2013 were eligible for inclusion. The interventions compared were posterior fossa decompression with duraplasty (PFDD) and posterior fossa decompression with bony decompression alone (PFD). Studies to be included were randomized controlled trials (RCTs) or quasi-RCTs (S1), but also observational studies (S2) including cohort studies, case–control studies or case series with ≥20 patients. This was decided as few or no S1 studies were expected, and S2 studies could supplement the evidence. Also, in the case of only low-quality evidence this strategy would effectively elucidate the need of performing better studies [12]. Further, we decided that the main meta-analysis should be performed with the S1 group while a supplementary analysis should be performed using the S2 cohort as long as the heterogeneity between studies remained acceptable (i.e. not approaching 100%). Also, detailed exclusion criteria are presented in the supplementary material. After the review of the literature it was apparent that no studies fulfilled criteria for S1 and therefore this systematic review consists only of S2-studies. 2.2. Data search A librarian (IIR) performed the searches in Embase, PubMed (includes MEDLINE), Cochrane Central Register of Controlled Trials (CENTRAL) and ClinicalTrials.gov. UpToDate was also screened for relevant articles.
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Only articles written or translated into English were included in this systematic review. The searches were run in the period September, 5–9 2013. The search details are presented in the supplementary material. Furthermore, reference lists of the reviewed articles were screened for additional relevant papers by the two investigators performing the review (ASJ, PF).
2.4.2. Sensitivity analysis If eligibility for some of the studies in the meta-analysis was questionable due to important sources of bias or lack of details, sensitivity analysis was planned by performing the meta-analysis both with and without these studies. 3. Results
2.3. Data extraction and management Data was extracted from included studies independently by two investigators (PF and ASJ) using a standardized data collection form. Cases of disagreement were solved by discussion, also including a third independent reviewer (OS). All variables in the data collection form are presented in the supplementary material. In case of overlapping or similar patient cohort reported in more than one publication the publication most suitable for this systematic review was included. In studies where other entities than CM1 were included (e.g. Chiari II or achondroplasia) and where the patient population consisted of both pediatric and adult patients the authors were contacted by e-mail in an attempt to extract data concerning patients fulfilling inclusion criteria for this systematic review. If we did not receive a reply a reminder was sent. If the reminder remained unanswered the study was excluded. 2.3.1. Primary end-point effect Proportions of patients re-operated due to clinical failure in the two groups.
The selection process is described in detail in Fig. 1. We retrieved 233 articles, but after the review process only 12 articles were included [1,5,10,15,16,18,22,23,25,26,28,30]. However, only four articles included posterior fossa decompression with both techniques (i.e. PFD vs PFDD) [10,16,22,30]. Thus, 8 of 12 articles for the purpose of our research question were case-series without control groups. Also, only 2 out of 12 articles had a prospective design, both comparing different duraplasty materials [18,28]. The characteristics of included studies are presented in Table 1 and the outcomes from individual studies are presented in Table 2. For each end-point in both treatment arms we tested heterogeneity to decide whether we could perform a meta-analysis of the observational studies. The heterogeneity was found to be less than 90% for all end-points. For details concerning heterogeneity see supplementary material. Based on the assumption that data from individual studies were similar enough to be grouped for the purpose of meta-analyses we merged all data into a PFDD group or PFD group. 3.1. Effectiveness of intervention
2.3.2. Primary end-point safety Proportions of patients with CSF related complications in the two groups. 2.3.3. Secondary end-point effect Proportions of clinical improvement (as defined by the researchers). Proportions of syringomyelia improvement as assessed by MRI. 2.3.4. Secondary end-point safety Proportions of re-operations due to CSF related complications. 2.4. Statistics We based our study on the Cochrane Handbook for Systematic Reviews of Interventions (edition 5.1.0. updated March 2011, www.cochrane-handbook.org). The review was prepared using RevManager version 5.1 (Cochrane Reviews) and I2 -statistics of observational studies were carried out with SPSS (version 18.0). Because only S2-studies were retrieved a random effect model was chosen because baseline, follow-up and outcome reporting were presumably different between studies. End-points were dichotomous and are presented as frequencies and odds ratio (OR) with 95% confidence interval (CI). 2.4.1. Assessment of heterogeneity Heterogeneity was assessed for each end-point in both treatment arms and tested by I2 which measured inconsistency (percentage of total variation across studies resulting from heterogeneity) of effects. In the event of >50% heterogeneity, we planned to use a random effect as described in the Cochrane Handbook for Systematic Reviews of Interventions. If severe heterogeneity (approximating 100%) was present for any end-point in either treatment group a meta-analysis would not be performed for that specific end-point.
Of the 432 surgeries in the PFDD group there were 8 (2%) re-operations due to clinical failure while there were 5 (11%) reoperations after the 46 in the PFD group. This is presented in Fig. 2. Lack of marked clinical improvement (as defined by researchers) was seen in 96 (23%) of 426 surgeries in the PFDD group. In the PFD group 11 (22%) of 51 had lack of improvement at the end of follow up, that is after the primary or secondary operations. This is presented in Fig. 3. In Fig. 4 we present the subgroup of patients with syringomyelia. In the PFDD group 65 (22%) of 298 surgeries did not lead to syringomyelia improvement assessed with postoperative MRI. In the PFD group 9 (26%) of 35 surgeries did not lead to syringomyelia improvement. 3.2. Cerebrospinal fluid related complications Figs. 5 and 6 summarize the CSF related complications between the treatments. In the PFDD group 32 (7%) of 472 surgeries lead to CSF related complication. In 18 (4%) of 438 surgeries invasive treatments were needed to repair the CSF leakage. None of the 41 patients in the PFD group had CSF related complications. 4. Discussion In this systematic review and meta-analysis of observational studies there were more re-operations due to lack of clinical improvement when PFD was performed compared to PFDD for CM1 in adults. However, at the end of follow up there were almost similar proportions of clinical improvement and syringomyelia improvement in both treatment groups. CSF related complications naturally occurred more frequent in the PFDD group, but the reviewed studies reported large variations in proportions of CSF related complications after PFDD. The difference in CSF-related complications between treatment groups was not statistically significant, but the low number of patients treated with PFD limits the statistical power of our meta-analysis.
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Fig. 1. Flow-chart of study inclusion.
Table 1 Characteristics of included studies. Authors
Year published
Duraplasty
Duraplasty type
No duraplasty
Prospective
Multi-center
Time to used follow-up (mo)
Mean age (y)
Aghakhani Batzdorf Erdogan Lam Lee Liu Munshi Sindou Spena Vanaclocha Williams Yilmaz SUM
2009 2013 2010 2013 2012 2005 2000 2002 2010 1997 2013 2011 –
151 26 15 22 20 40 14 44 36 26 34 58 486
Mix Mix Artificial Autologous Mix Mix Mix Autologous Unknown Mix Mix Mix –
0 0 12 0 5 0 10 0 0 0 0 24 51
No No No No No Yes No No No No Yes No 2/12
No No No No No No No No No No No No 0/12
88 89 NA 12 48 NA 6 12 40 6 3 9 –
38.3 NA 25.9 37.3 36.6 41.4 NA 40.0 40.4 28.5 38.7 38.9 –
Fig. 2. Re-operations due to clinical failure in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
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Table 2 Summary of results. Authors
PFDDa total
Re-opb
Failurec
Syrinxd
CSF relatede
CSF re-opf
PFDg total
Re-op
Failure
Syrinx
CSF related
CSF re-op
Aghakhani Batzdorf Erdogan Lam Lee Liu Munshi Sindou Spena Vanaclocha Williams Yilmaz
151 26 15 22 20 40 14 44 36 26 34 58
6/151 0/26 0/15 0/22 ?/20 0/40 0/14 0/44 2/36 0/26 ?/34 0/58
58/151 ?/26 4/15 1/22 0/20 6/40 3/14 8/44 7/36 3/26 ?/34 6/58
38/150 1/16 3/11 ?/? 6/20 ?/40 0/5 6/15 7/36 0/0 ?/? 4/45
7/151 0/26 3/15 1/22 0/20 0/40 ?/14 2/44 3/36 7/26 5/34 4/58
1/151 0/26 3/15 1/22 0/20 0/40 ?/14 1/44 3/36 7/26 ?/34 2/58
0 0 12 0 5 0 10 0 0 0 0 24
N/A N/A 1/12 0 ?/5 0 2/10 0 0 0 0 2/24
N/A N/A 2/12 N/A 1/5 N/A 3/10 N/A N/A N/A N/A 5/24
N/A N/A 0/4 N/A 2/5 N/A 4/7 N/A N/A N/A N/A 3/19
N/A N/A 0/12 N/A 0/5 N/A ?/10 N/A N/A N/A N/A 0/24
N/A N/A 0/12 N/A 0/5 N/A ?/10 N/A N/A N/A N/A 0/24
a b c d e f g
PFDD—group treated with posterior fossa decompression and duraplasty. Re-op—re-operated due to clinical failure. Failure—patients showing lack of improvement at end of follow-up. Syrinx—failure of syrinx regression assessed with postoperative MRI (independent of timing of assessment postoperatively). CSF related—complications possibly related to CSF (leakage, symptomatic pseudomeningocele, meningitis). CSF re-op—need of procedure to solve CSF related problems (e.g. lumbar drainage or re-operation). PFD—group treated with posterior fossa decompression alone without duraplasty.
Fig. 3. Patients failed to improve (as defined by the researchers) in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
Fig. 4. Failed to improve syringomyelia as assessed with postoperative MRI scan in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
Fig. 5. CSF related complications in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
Although this systematic review reveals higher reoperation rates in the PFD group, no apparent difference in lack of clinical improvement was seen between the two surgical techniques at the end of follow-up. However, more patients needed complementary surgery in the PFD group. Regardless of technique, a proportion of patients will remain symptomatic after posterior fossa decompression. Reasons may be wrong diagnosis, a chronic irreversible
pain conditions or medical or surgical complications leading to persistence of symptoms. If only PFD has been performed, reoperation with durotomy with subsequent duraplasty remains as an option. Thus, this unused treatment option may inflate the number of re-operations due to clinical failure in the PFD group. Where adequate PFDD was performed upfront and the patient fails to improve, no further surgical decompression can usually be
Fig. 6. Re-operations due to CSF related complications in relation to decompression procedure (bony decompression and duraplasty versus bony decompression alone without duraplasty).
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offered. Unfortunately, the included studies offer no insight into the success rates of re-operations with duroplasty after unsuccessful PFD. Although the difference in CSF complication rates between 7% and 0% after PFDD and PFD did not reach statistical significance, it is still likely that opening the meninges will increase CSF complication rates. From this systematic review we are unable to draw any conclusion on which technique that provides the best clinical outcome. Thus a staged approach in elective decompressive surgery for CM1 with PFD remains a feasible option, to minimize the risk of CSF complications. Using this approach a systematic and thorough follow-up is however required because some patients may require reoperations with duraplasty. Compared to the pediatric meta-analysis of decompressive surgery for CM1 the results in this meta-analysis on adult CM1 patients are fairly similar [9]. In the pediatric patients treated with PFDD 2.1% had re-operations compared to 12.6% in patients treated with PFD (2% and 11% in this meta-analysis, respectively). Although not statistically significant in the pediatric population more patients seemed to experience improvement (78.6% in PFDD vs 64.6% in PFD) and syringomyelia resolution (87% in PFDD vs 56.3% in PFD) after duraplasty. The proportions from our meta-analysis in adults were 77% in PFDD versus 78% in PFD for clinical improvement. Moreover, 78% treated with PFDD versus 74% treated with PFD experienced syringomyelia improvement as assessed with MRI. CSF related complications related to PFDD were seen in 19% of the pediatric surgeries compared to 7% after surgery in the adult population. Thus, it seems like both the effect of PFD and safety of PFDD is better in adult patients. The possibility remains that there is no universal strategy in decompressive surgery of CM1 patients. There may be useful tools for a tailored approach available, but further clinical validation is necessary. Electrophysiological studies have demonstrated that conduction time improvement in pediatric patients was most pronounced after bony decompression and division of the atlantooccipital membrane, with only slight or no additional improvement after duraplasty [4,32]. To what extent these indirect measures translate into clinical benefit remains unanswered, but these findings suggest that bony decompression alone may suffice in pediatric patients. Intraoperative ultrasound can be another tool of interest when attempting to tailor the approach [6,19]. Highfrequency probes clearly visualize the anatomy and when using color Doppler detailed flow-measurements are possible. In children it has been demonstrated that if CSF is pulsating behind the cerebellar tonsils after bony decompression further decompression with dural opening may not be necessary [29,31]. However, further systematic evaluation of the intraoperative findings encountered with electrophysiology and intraoperative ultrasound is needed before we can recommend using the techniques as routine guidance. After completed systematic search of literature and inclusion a recent study of 47 consecutive adults patients treated with PFD with long-term follow-up was published [14]. The mean followup was 111 months, longer than in all other included studies in the present review. The authors found long-term clinical improvement in approximately 60% of patients, and approximately 32% required reoperation with additional decompression. The first impression is that this failure rate seems high, but long-term improvement in the PFDD case series with longest follow-up (median 88 months) included in the present systematic review was 63% [1]. However, only 4% in that study underwent repeated decompression. The limitations of the existing literature represent the main limitation of this systematic review. There are no randomized studies or pseudo-randomized trials. The limited number of studies, the observational and retrospective character of most included studies, and the heterogeneity of studies must be taken into account when interpreting results from this systematic review. There were also few observational studies with bony decompression alone (PFD
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group) that were eligible for inclusion. Also, 10 out of 12 included articles were retrospective with large variation in time to assessment between studies. In this case, the retrospective observational design and different follow up time of the included studies could affect proportions of clinical failure, but presumably the safety endpoints are less vulnerable in this regard. As eligibility for some of the studies in the meta-analysis was questionable due to important sources of bias or lack of details, sensitivity analysis was planned by performing the meta-analysis both with and without these studies. In the absence of high-quality studies, we decided against classifying the low-quality evidence further into more or less reliable. Assessment of publication bias was performed reporting proportion versus sample size in a funnel plot, but with only 12 studies included a reliable interpretation is difficult (see online material). Still, we did not find any clear indication of publication bias based on this assessment. According to the manual for systematic reviews, inclusion of observational studies is discouraged, due to the inherent risk of bias in these reports. Even with a sophisticated systematic review protocol, the results from the meta-analysis will not be more reliable than the data extracted from the individual studies (www.cochrane-handbook.org). This point to a general problem of systematic reviews and meta-analyses when high evidence studies are lacking, which is often the case in neurosurgery. We are not attempting scientific alchemy by drawing firm conclusions from uncontrolled observational data [7,8,24], but our review highlights the need of performing properly controlled studies on surgical techniques in CM1 patients. To reassure an indisputable endpoint in this heterogeneous material we used risk of reoperation as primary endpoint. However, there is reason to believe that reoperation is more likely to be recommended for patients with lack of improvement in the PFD group, compared to patients with clinical failure treated with PFDD, where fewer treatment options are available. In the end, the chance of clinical improvement was similar, but more patients in the PFD group needed a second operation to achieve this improvement.
5. Conclusion Although this systematic review of observational studies reveals higher reoperation rates with bony decompression alone, clinical improvement was not higher after primary decompression with duroplasty. Since the majority of patients will improve with PFD without duraplasty, a staged approach is still feasible to avoid CSF related complications. On the other hand the safety profile of PFDD in adults is better than in children, making this approach feasible if low complication rates can be documented. However, we encourage more systematic use of tools with subsequent systematic clinical assessments in an attempt to tailor the approach. At present there are no high-quality studies to offer guidance in the choice of decompressive technique in adult CM1 patients and we see no reasons why a RCT on surgical technique cannot be performed in non-emergent adult cases with CM1.
Author role Petter Förander: planning, revising protocol, data registration, analysis, interpretation, drafting article, submission of article. Kristin Sjåvik: publishing protocol (PROSPERO), interpretation, revising article. Ole Solheim: planning, revising protocol, data interpretation, revising article. Ingrid Riphagen: planning, revising protocol, systematic search and paper identification. Sasha Gulati: data interpretation, revising article.
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Øyvind Salvesen: planning, statistical supervision, revising article. Asgeir Store Jakola: planning, writing protocol, data registration, analysis and interpretation, drafting article, revising article, supervision. Protocol registration: PROSPERO 2013:CRD42013006252. Funding source None. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.clineuro. 2014.07.019. References [1] Aghakhani N, Parker F, David P, Morar S, Lacroix C, Benoudiba F, et al. Long-term follow-up of Chiari-related syringomyelia in adults: analysis of 157 surgically treated cases. Neurosurgery 2009;64:308–15. [2] Alden TD, Ojemann JG, Park TS. Surgical treatment of Chiari I malformation: indications and approaches. Neurosurg Focus 2001;11:E2. [3] Alfieri A, Pinna G. Long-term results after posterior fossa decompression in syringomyelia with adult Chiari Type I malformation. J Neurosurg Spine 2012;17:381–7. [4] Anderson RC, Emerson RG, Dowling KC, Feldstein NA. Improvement in brainstem auditory evoked potentials after suboccipital decompression in patients with Chiari I malformations. J Neurosurg 2003;98:459–64. [5] Batzdorf U, McArthur DL, Bentson JR. Surgical treatment of Chiari malformation with and without syringomyelia: experience with 177 adult patients. J Neurosurg 2013;118:232–42. [6] Cui LG, Jiang L, Zhang HB, Liu B, Wang JR, Jia JW, et al. Monitoring of cerebrospinal fluid flow by intraoperative ultrasound in patients with Chiari I malformation. Clin Neurol Neurosurg 2011;113:173–6. [7] De Witt Hamer PC, Gil Robles S, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a metaanalysis. J Clin Oncol 2012;30:2559–65. [8] Duffau H. The conceptual limitation to rely on intraoperative MRI in glioma surgery. World Neurosurg 2014 [Epub ahead of print]. [9] Durham SR, Fjeld-Olenec K. Comparison of posterior fossa decompression with and without duraplasty for the surgical treatment of Chiari malformation Type I in pediatric patients: a meta-analysis. J Neurosurg Pediatr 2008;2:42–9. [10] Erdogan E, Cansever T, Secer HI, Temiz C, Sirin S, Kabatas S, et al. The evaluation of surgical treatment options in the Chiari malformation type I. Turk Neurosurg 2010;20:303–13. [11] Hankinson T, Tubbs RS, Wellons J. Duraplasty or not? An evidence-based review of the pediatric Chiari I malformation. Child’s Nerv Syst 2011;27:35–40. [12] Ijaz S, Verbeek JH, Mischke C, Ruotsalainen J. Inclusion of nonrandomized studies in Cochrane systematic reviews was found to be in need of improvement. J Clin Epidemiol 2014;67:645–53. [13] Kalb S, Perez-Orribo L, Mahan M, Theodore N, Nakaji P, Bristol RE. Evaluation of operative procedures for symptomatic outcome after decompression surgery for Chiari type I malformation. J Clin Neurosci 2012;19:1268–72.
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