Complications and outcomes of posterior fossa decompression with duraplasty versus without duraplasty for pediatric patients with Chiari malformation type I and syringomyelia: a study from the Park-Reeves Syringomyelia Research Consortium

S. Hassan A. Akbari MD, MS1, Alexander T. Yahanda MD2, Laurie L. Ackerman MD3, P. David Adelson MD4, Raheel Ahmed MD, PhD5, Gregory W. Albert MD, MPH6, Philipp R. Aldana MD7, Tord D. Alden MD8, Richard C. E. Anderson MD9, David F. Bauer MD10, Tammy Bethel-Anderson2, Karin Bierbrauer MD36, Douglas L. Brockmeyer MD11, Joshua J. Chern MD, PhD12, Daniel E. Couture MD13, David J. Daniels MD, PhD14, Brian J. Dlouhy MD15, Susan R. Durham MD16, Richard G. Ellenbogen MD17, Ramin Eskandari MD18, Herbert E. Fuchs MD, PhD19, Gerald A. Grant MD20, Patrick C. Graupman MD21, Stephanie Greene MD22, Jeffrey P. Greenfield MD, PhD23, Naina L. Gross MD24, Daniel J. Guillaume MD25, Todd C. Hankinson MD26, Gregory G. Heuer MD, PhD27, Mark Iantosca MD1, Bermans J. Iskandar MD5, Eric M. Jackson MD28, George I. Jallo MD29, James M. Johnston MD30, Bruce A. Kaufman MD31, Robert F. Keating MD32, Nicklaus R. Khan MD33, Mark D. Krieger MD16, Jeffrey R. Leonard MD34, Cormac O. Maher MD35, Francesco T. Mangano DO36, J. Gordon McComb MD16, Sean D. McEvoy MD2, Thanda Meehan RN2, Arnold H. Menezes MD15, Michael S. Muhlbauer MD33, Brent R. O’Neill MD26, Greg Olavarria MD37, John Ragheb MD38, Nathan R. Selden MD, PhD39, Manish N. Shah MD40, Chevis N. Shannon DrPH41, Joshua S. Shimony MD, PhD42, Matthew D. Smyth MD29, Scellig S. D. Stone MD, PhD43, Jennifer M. Strahle MD2, Mandeep S. Tamber MD, PhD44, James C. Torner PhD15, Gerald F. Tuite MD29, Elizabeth C. Tyler-Kabara MD, PhD45, Scott D. Wait MD46, John C. Wellons III MD, MSPH41, William E. Whitehead MD10, Tae Sung Park MD2, and David D. Limbrick Jr. MD, PhD2
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  • 1 Division of Pediatric Neurosurgery, Penn State Health Children’s Hospital, Hershey, PA;
  • | 2 Department of Neurological Surgery, Washington University School of Medicine, St. Louis, MO;
  • | 3 Department of Neurological Surgery, Indiana University School of Medicine, Indianapolis, IN;
  • | 4 Division of Pediatric Neurosurgery, Barrow Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ;
  • | 5 Department of Neurological Surgery, University of Wisconsin at Madison, Madison, WI;
  • | 6 Division of Neurosurgery, Arkansas Children’s Hospital, Little Rock, AR;
  • | 7 Division of Pediatric Neurosurgery, University of Florida College of Medicine, Jacksonville, FL;
  • | 8 Division of Pediatric Neurosurgery, Ann and Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL;
  • | 9 Division of Pediatric Neurosurgery, Department of Neurological Surgery, Children’s Hospital of New York, Columbia-Presbyterian, New York, NY;
  • | 10 Division of Pediatric Neurosurgery, Texas Children’s Hospital, Houston, TX;
  • | 11 Division of Pediatric Neurosurgery, Primary Children’s Hospital, Salt Lake City, UT;
  • | 12 Division of Pediatric Neurosurgery, Children’s Healthcare of Atlanta University, Atlanta, GA;
  • | 13 Department of Neurological Surgery, Wake Forest University School of Medicine, Winston-Salem, NC;
  • | 14 Department of Neurosurgery, Mayo Clinic, Rochester, MN;
  • | 15 Department of Neurosurgery, University of Iowa Hospitals and Clinics, Iowa City, IA;
  • | 16 Division of Pediatric Neurosurgery, Children’s Hospital of Los Angeles, Los Angeles, CA;
  • | 17 Division of Pediatric Neurosurgery, Seattle Children’s Hospital, Seattle, WA;
  • | 18 Department of Neurosurgery, Medical University of South Carolina, Charleston, SC;
  • | 19 Department of Neurosurgery, Duke University School of Medicine, Durham, NC;
  • | 20 Division of Pediatric Neurosurgery, Lucile Packard Children’s Hospital, Palo Alto, CA;
  • | 21 Division of Pediatric Neurosurgery, Gillette Children’s Hospital, St. Paul, MN;
  • | 22 Division of Pediatric Neurosurgery, Children’s Hospital of Pittsburgh, University of Pittsburgh Medical Center, Pittsburgh, PA;
  • | 23 Department of Neurological Surgery, Weill Cornell Medical College, NewYork-Presbyterian Hospital, New York, NY;
  • | 24 Department of Neurosurgery, University of Oklahoma, Oklahoma City, OK;
  • | 25 Department of Neurosurgery, University of Minnesota Medical School, Minneapolis, MN;
  • | 26 Department of Neurosurgery, Children’s Hospital Colorado, Aurora, CO;
  • | 27 Division of Pediatric Neurosurgery, Children’s Hospital of Philadelphia, Philadelphia, PA;
  • | 28 Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD;
  • | 29 Division of Neurosurgery, Johns Hopkins All Children’s Hospital, St. Petersburg, FL;
  • | 30 Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL;
  • | 31 Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, WI;
  • | 32 Department of Neurosurgery, Children’s National Medical Center, Washington, DC;
  • | 33 Department of Neurosurgery, The University of Tennessee Health Science Center, Memphis, TN;
  • | 34 Division of Pediatric Neurosurgery, Nationwide Children’s Hospital, Columbus, OH;
  • | 35 Department of Neurosurgery, University of Michigan, Ann Arbor, MI;
  • | 36 Division of Pediatric Neurosurgery, Cincinnati Children’s Medical Center, Cincinnati, OH;
  • | 37 Division of Pediatric Neurosurgery, Arnold Palmer Hospital for Children, Orlando, FL;
  • | 38 Department of Neurological Surgery, University of Miami School of Medicine, Miami, FL;
  • | 39 Department of Neurological Surgery and Doernbecher Children’s Hospital, Oregon Health & Science University, Portland, OR;
  • | 40 Division of Pediatric Neurosurgery, McGovern Medical School, Houston, TX;
  • | 41 Division of Pediatric Neurosurgery, Monroe Carell Jr. Children’s Hospital at Vanderbilt University, Nashville, TN;
  • | 42 Department of Radiology, Washington University School of Medicine, St. Louis, MO;
  • | 43 Division of Pediatric Neurosurgery, Boston Children’s Hospital, Boston, MA;
  • | 44 Division of Neurosurgery, The University of British Columbia, Vancouver, BC, Canada;
  • | 45 Department of Neurosurgery, The University of Texas at Austin, Austin, TX; and
  • | 46 Carolina Neurosurgery & Spine Associates, Charlotte, NC
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OBJECTIVE

The aim of this study was to determine differences in complications and outcomes between posterior fossa decompression with duraplasty (PFDD) and without duraplasty (PFD) for the treatment of pediatric Chiari malformation type I (CM1) and syringomyelia (SM).

METHODS

The authors used retrospective and prospective components of the Park-Reeves Syringomyelia Research Consortium database to identify pediatric patients with CM1-SM who received PFD or PFDD and had at least 1 year of follow-up data. Preoperative, treatment, and postoperative characteristics were recorded and compared between groups.

RESULTS

A total of 692 patients met the inclusion criteria for this database study. PFD was performed in 117 (16.9%) and PFDD in 575 (83.1%) patients. The mean age at surgery was 9.86 years, and the mean follow-up time was 2.73 years. There were no significant differences in presenting signs or symptoms between groups, although the preoperative syrinx size was smaller in the PFD group. The PFD group had a shorter mean operating room time (p < 0.0001), fewer patients with > 50 mL of blood loss (p = 0.04), and shorter hospital stays (p = 0.0001). There were 4 intraoperative complications, all within the PFDD group (0.7%, p > 0.99). Patients undergoing PFDD had a 6-month complication rate of 24.3%, compared with 13.7% in the PFD group (p = 0.01). There were no differences between groups for postoperative complications beyond 6 months (p = 0.33). PFD patients were more likely to require revision surgery (17.9% vs 8.3%, p = 0.002). PFDD was associated with greater improvements in headaches (89.6% vs 80.8%, p = 0.04) and back pain (86.5% vs 59.1%, p = 0.01). There were no differences between groups for improvement in neurological examination findings. PFDD was associated with greater reduction in anteroposterior syrinx size (43.7% vs 26.9%, p = 0.0001) and syrinx length (18.9% vs 5.6%, p = 0.04) compared with PFD.

CONCLUSIONS

PFD was associated with reduced operative time and blood loss, shorter hospital stays, and fewer postoperative complications within 6 months. However, PFDD was associated with better symptom improvement and reduction in syrinx size and lower rates of revision decompression. The two surgeries have low intraoperative complication rates and comparable complication rates beyond 6 months.

ABBREVIATIONS

AP = anteroposterior; CM1 = Chiari malformation type I; CXA = clivoaxial angle; pBC2 = a line perpendicular to a line from the basion to the posteroinferior aspect of the C2 body; PFD = posterior fossa decompression; PFDD = PFD with duraplasty; PRSRC = Park-Reeves Syringomyelia Research Consortium; SM = syringomyelia.

OBJECTIVE

The aim of this study was to determine differences in complications and outcomes between posterior fossa decompression with duraplasty (PFDD) and without duraplasty (PFD) for the treatment of pediatric Chiari malformation type I (CM1) and syringomyelia (SM).

METHODS

The authors used retrospective and prospective components of the Park-Reeves Syringomyelia Research Consortium database to identify pediatric patients with CM1-SM who received PFD or PFDD and had at least 1 year of follow-up data. Preoperative, treatment, and postoperative characteristics were recorded and compared between groups.

RESULTS

A total of 692 patients met the inclusion criteria for this database study. PFD was performed in 117 (16.9%) and PFDD in 575 (83.1%) patients. The mean age at surgery was 9.86 years, and the mean follow-up time was 2.73 years. There were no significant differences in presenting signs or symptoms between groups, although the preoperative syrinx size was smaller in the PFD group. The PFD group had a shorter mean operating room time (p < 0.0001), fewer patients with > 50 mL of blood loss (p = 0.04), and shorter hospital stays (p = 0.0001). There were 4 intraoperative complications, all within the PFDD group (0.7%, p > 0.99). Patients undergoing PFDD had a 6-month complication rate of 24.3%, compared with 13.7% in the PFD group (p = 0.01). There were no differences between groups for postoperative complications beyond 6 months (p = 0.33). PFD patients were more likely to require revision surgery (17.9% vs 8.3%, p = 0.002). PFDD was associated with greater improvements in headaches (89.6% vs 80.8%, p = 0.04) and back pain (86.5% vs 59.1%, p = 0.01). There were no differences between groups for improvement in neurological examination findings. PFDD was associated with greater reduction in anteroposterior syrinx size (43.7% vs 26.9%, p = 0.0001) and syrinx length (18.9% vs 5.6%, p = 0.04) compared with PFD.

CONCLUSIONS

PFD was associated with reduced operative time and blood loss, shorter hospital stays, and fewer postoperative complications within 6 months. However, PFDD was associated with better symptom improvement and reduction in syrinx size and lower rates of revision decompression. The two surgeries have low intraoperative complication rates and comparable complication rates beyond 6 months.

In Brief

The Park-Reeves Syringomyelia Research Consortium database was used to compare complications and outcomes between posterior fossa decompression with and without duraplasty for Chiari I malformations. The authors found that posterior fossa decompression was associated with fewer complications and shorter hospital stays than posterior fossa decompression with duraplasty, although it was associated with a higher revision rate and lower rates of headache and syrinx improvement. This study, coupled with the forthcoming results of a randomized controlled trial, should help improve understanding regarding the indications for each surgery.

Chiari malformation type I (CM1) is a common pediatric neurosurgical disease characterized by ectopia of the cerebellar tonsils below the level of the foramen magnum and is often associated with syringomyelia (SM).1–4 Controversy continues regarding the treatment of CM1-SM by posterior fossa decompression with duraplasty (PFDD) versus extradural posterior fossa decompression (PFD).5–20 A number of single-institution studies and meta-analyses have evaluated PFD and PFDD in terms of complication rates, improvement in clinical symptoms, and reduction in syrinx size,5,18,21,22 but there have been no large-scale multicenter prospective or retrospective studies comparing PFD and PFDD in the pediatric population.

To address this critical void in the literature regarding pediatric CM1-SM, we conducted a retrospective analysis comparing PFD with PFDD using a large multicenter cohort of pediatric patients who underwent PFD or PFDD for CM1-SM at medical institutions across North America. Our primary research aim was to clarify differences in postoperative complications between PFD and PFDD, while our secondary research aim was to discern differences in postoperative syrinx size, symptom improvement, physical examination changes, and operative parameters between the two groups. To our knowledge, this is the largest study examining complication rates, postoperative outcomes, and other differences between PFD and PFDD for CM1-SM.

Methods

This study was a retrospective examination of retrospectively and prospectively acquired data in the Park-Reeves Syringomyelia Research Consortium (PRSRC) registry. The PRSRC is a multicenter research collaborative created to improve the understanding of CM1-SM and its treatment. Starting in 2011, the PRSRC has worked to collect data both retrospectively (from July 2011 to October 2014) and prospectively (since October 2014), with a total of 42 contributing centers. All study-related procedures were approved by institutional review boards at the host institution (Washington University in St. Louis Human Research Protection Office) and each participating center. For this study, patients were enrolled retrospectively and prospectively from surgery. Patients had their initial consultation for neurosurgical evaluation between September 2001 and February 2018. All patients had tonsillar ectopia ≥ 5 mm, syrinx diameter ≥ 3 mm, and ≥ 1-year postoperative follow-up from their index decompression procedure. The type of surgical intervention performed was at the discretion of the treating physician. Patients without documented SM; those older than 21 years of age; and those with Chiari malformation types II, III, and IV were excluded from the study. Presenting patient demographics, clinical signs and symptoms, surgical parameters, complications, and improvement in signs and symptoms were compiled and analyzed. Before data entry into the PRSRC registry, a signed consent form was required and obtained for all prospectively enrolled patients. A waiver of consent was obtained for retrospectively enrolled patients. For this current study, 349 patients (50.4%) were prospectively enrolled and 343 patients (49.6%) were retrospectively enrolled (Table 1). There were no differences between the retrospective and prospective cohorts for mean age at surgery (p = 0.75), mean follow-up time (p = 0.44), and sex (p = 0.2). The prospective cohort was more likely to receive PFDD (86.5%) compared with the retrospective cohort (79.6%) (p = 0.01).

TABLE 1.

Demographics of all patients stratified by treatment type

VariablePFDPFDDp Value
No. of pts117575
 Prospectively collected48 (41.0)301 (52.3)0.03
 Retrospectively collected69 (59.0)274 (47.7)
Mean age at op, yrs9.46 ± 4.149.94 ± 4.640.26
Mean follow-up, yrs2.73 ± 1.122.72 ± 1.160.93
Sex
 Male54 (46.2)224 (39.0)0.15
 Female63 (53.8)351 (61.0)
Race
 White88 (75.2)480 (83.5)0.05
 Black7 (6.0)60 (10.4)0.14
 Asian3 (2.6)7 (1.2)0.27
 Hispanic or Latino23 (19.7)62 (10.8)0.01
 Native American0 (0.0)2 (0.3)>0.99
Insurance
 Private77 (65.8)403 (70.1)0.36
 Medicaid38 (32.5)180 (31.3)0.80
 Self-pay/no insurance3 (2.6)11 (1.9)0.71

Pt = patient. Values represent the number of patients (%) unless stated otherwise. Mean values are presented as mean ± SD. Boldface type indicates statistical significance.

Data Collection and Consistency

Demographic data, clinical symptoms, physical examination findings, and radiological measurements were collected and recorded in the PRSRC database at both pre- and postoperative encounters.

The data dictionary comprised 24 sections across multiple domains, including social and demographic parameters, preoperative and postoperative symptoms, treatment parameters, radiographic parameters, and outcome parameters. Most data elements offered specific designations (“yes/no,” “improved/stable/worse”). The same variables for each section were used for every subject at every site to ensure data consistency throughout the study. A data monitor at the lead PRSRC site (Washington University in St. Louis) remotely reviewed the completed data set for each participant as they were enrolled and with each follow-up visit. Sites were reimbursed for each participant enrolled but only after all data elements in the data dictionary were complete and all neuroimaging was uploaded to the Centralized Neuroimaging Data Archive. Radiological images for all PRSRC patients have been reviewed by two blinded, trained readers, one of whom is a board-certified pediatric neuroradiologist.

Radiological measurements included syrinx diameter in the anteroposterior (AP) dimension (mm), syrinx length (as measured in vertebral levels), tonsillar descent (in mm), clivoaxial angle (CXA), and a line perpendicular to a line from the basion to the posteroinferior aspect of the C2 body (pBC2; in mm). Clinical symptoms were subdivided into categories corresponding to headaches (including headache location), nausea/vomiting, visual disturbances, cranial nerve symptoms, subaxial pain (including upper- and lower-extremity pain, neck pain, back pain, and trunk pain), spinal cord symptoms, and cerebellar symptoms. Clinical signs were subdivided into categories corresponding to lethargy and papilledema, cranial nerve signs, spinal cord signs (weakness, reflexes, sensation, and proprioception), and cerebellar signs. Postoperative complications included pseudomeningocele, CSF leak or drainage, meningitis (chemical or infectious), hydrocephalus, infection, cervical instability (with any fusion procedures), and ventriculoperitoneal shunt requirement. Pseudomeningocele was diagnosed based on having both clinical signs or symptoms and positive imaging. They may have been treated conservatively or surgically. Asymptomatic pseudomeningoceles were not included. Chemical meningitis was diagnosed from clinical signs and symptoms with a negative CSF culture. Infectious meningitis was diagnosed from clinical signs and symptoms with a culture-positive lumbar puncture and antibiotic treatment.

Statistical Analysis

Comparisons between the PFD and PFDD groups were performed for demographic data, symptoms, physical examination findings, radiological measurements, postoperative complications, and intraoperative data. The Student t-test and the Mann-Whitney U-test were used to compare continuous variables (e.g., syrinx size, changes in radiological measurements, and mean hospital stay). A two-sided p value < 0.05 was considered statistically significant for all statistical tests. Odds ratios were calculated with 95% confidence intervals. The reference group was PFDD. All statistical analyses were performed using SAS version 9.4 (SAS Institute, Inc.) and Stata version 16.1 (StataCorp). Chi-square and Fisher’s exact tests were used to compare categorical variables (e.g., differences in complication rates or differences in the rates of symptoms or physical examination findings).

Results

A total of 692 patients met inclusion criteria: 117 (16.9%) underwent PFD and 575 (83.1%) underwent PFDD. Among all patients, 414 (59.8%) were female. The mean age at surgery for the cohort was 9.86 ± 4.56 years, and the mean follow-up time for all patients was 2.73 ± 1.16 years. The mean age at time of surgery and mean follow-up time did not significantly differ between the PFD and PFDD groups (p = 0.26 and p = 0.93, respectively). Demographic information for the individual groups is listed in Table 1.

Presenting Signs and Symptoms

The differences between groups for presenting signs and symptoms are listed in Table 2. For presenting symptoms, the only statistically significant difference between groups was for the proportion of patients who presented with holocranial headaches (26.5% PFD vs 14.6% PFDD, p = 0.003). For presenting physical examination findings, neck rotation weakness (4.3% PFD vs 1.0% PFDD, p = 0.02) was significantly different between groups, although the overall number of patients with this symptom was too small to make meaningful comparisons. No other presenting symptoms or examination findings significantly differed between groups.

TABLE 2.

Presenting symptoms and examination findings

VariableNo. of Ptsp ValueOR*95% CI
PFD (n = 117)PFDD (n = 575)
Symptoms
 Headache
  Occipital/suboccipital261380.680.900.54–1.48
  Frontal12690.750.840.40–1.63
  Holocranial31840.0032.111.27–3.44
  Parietal2130.710.750.08–3.40
  Temporal2180.550.540.06–2.30
  Worse w/ Valsalva8570.380.670.27–1.46
 Nausea/vomiting4460.110.410.10–1.15
 Cranial nerve
  Double vision4210.900.930.23–2.84
  Facial numbness190.560.540.01–3.98
  Facial weakness140.851.230.02–12.68
  Difficulty swallowing11620.740.860.39–1.71
  Hoarseness170.740.700.01–5.53
  Choking7300.661.160.42–2.77
  Vocal cord dysfunction190.560.540.01–3.98
  Sleep apnea7240.461.460.52–3.60
 Subaxial pain
  Upper-extremity pain5280.780.870.26–2.36
  Lower-extremity pain4350.250.550.14–1.57
  Neck pain24990.431.240.72–2.08
  Back pain22890.411.260.72–2.16
  Trunk pain0100.23
 Spinal cord
  Incontinence4360.280.530.13–1.52
 Cerebellar
  Tremors390.441.650.28–6.77
  Balance/gait ataxia17840.980.990.53–1.78
Exam findings
 Lethargic/stuporous01>0.99
 Papilledema050.59
 Cranial nerve
  Nystagmus5390.410.610.18–1.61
  Dysconjugate gaze2100.980.980.10–4.70
  Extraocular palsies130.521.640.03–20.66
  Facial weakness050.59
  Decreased facial sensation090.17
  Hearing loss3130.741.130.20–4.23
  Hoarseness03>0.99
  Tongue deviation110.314.950.06–389.06
  Weak gag8330.671.200.47–2.75
  Weak shrug100.17
  Weak neck rotation560.024.231.01–16.92
 Spinal cord
  Upper-extremity weakness7240.461.460.52–3.60
  Lower-extremity weakness4180.781.090.26–3.41
  Light touch deficit5390.410.610.18–1.61
  Pinprick deficit3300.340.480.09–1.58
  Joint position deficit03>0.99
  Deep tendon reflexes
   Absent6270.811.100.36–2.80
   Hypoactive634>0.990.860.29–2.14
   Hyperactive13510.481.280.62–2.50
  Ankle clonus4180.781.090.26–3.41
  Babinski reflex2130.710.750.08–3.39
  Hoffman’s reflex3120.731.230.22–4.67
 Cerebellar
  Gait instability10570.730.850.37–1.75
  Romberg response240.272.480.22–17.52
  Dysmetria1120.710.400.01–2.79

Boldface type indicates statistical significance.

The reference group is PFDD.

Complications and Operative Parameters

The intraoperative complication rate was low (0.0% PFD vs 0.7% PFDD, p > 0.99), and the rate of complications beyond 6 months after surgery was comparable (0.9% PFD vs 2.8% PFDD, p = 0.33) between groups; however, PFD yielded significantly fewer complications within 6 months after surgery (13.7% PFD vs 24.3% PFDD, p = 0.01). When analyzing individual types of complications, patients who underwent PFDD were found to have a significantly higher rate of clinically significant postoperative pseudomeningocele than those who underwent PFD (7.7% PFDD vs 2.6% PFD, p = 0.04). No other specific postoperative complications were different between groups. Data regarding intraoperative and postoperative complications are listed in Table 3 (refer to Data Collection and Consistency above).

TABLE 3.

Intraoperative complications and complications within and beyond 6 months

VariablePFD (n = 117)PFDD (n = 575)p ValueOR*95% CI
No. of pts w/ intraop complications (%)0 (0)4 (0.7)>0.99
 Vascular injury02>0.99
 Hemorrhage02>0.99
 Neurological injury02>0.99
 Death00
 Other complications03>0.99
No. of pts w/ complications w/in 6 mos (%)16 (13.7)140 (24.3)0.010.490.26–0.87
 Pseudomeningocele3440.040.320.06–0.94
 CSF leak5350.520.690.21–1.82
 Received surgical treatment (wound oversewing or surgical wound revision)419>0.991.030.24–3.20
 Received no surgical treatment1160.330.300.01–1.98
 External CSF drainage required2170.750.570.05–2.46
 Meningitis2250.180.380.04–1.57
  Chemical meningitis2200.320.480.05–2.03
  Infectious meningitis050.59
 Postop hydrocephalus1120.710.400.01–2.79
 Cervical instability130.521.640.03–20.66
 Managed w/ cervical collar120.432.470.04–47.73
 Necessitating fusion01>0.99
 Infection220.134.980.36–69.14
No. of pts w/ complications beyond 6 mos (%)1 (0.9)16 (2.8)0.330.300.01–1.98
 Cervical instability01>0.99
 Fusion requirement01>0.99
 Infection01>0.99
 Pseudomeningocele03>0.99
 Hydrocephalus03>0.99
 Shunt placement02>0.99
 Syrinx shunt placement15>0.990.980.02–8.90

Boldface type indicates statistical significance.

The reference group is PFDD.

The mean operating room time was shorter for the PFD group (1.98 ± 1.06 hours) than for the PFDD group (2.92 ± 1.32 hours) (p < 0.0001). The number of patients with > 50 mL of blood loss was greater in the PFDD group (18.3%) compared with the PFD group (10.2%) (p = 0.04). The mean length of hospital stay was shorter in the PFD group (3.45 ± 2.58 days) than in the PFDD group (4.57 ± 3.70 days) (p = 0.0001). There were no differences between the groups in terms of need for postdecompression shunting (p = 0.41) or fusion (p = 0.54). The PFD group was more likely to require revision surgery compared with the PFDD group (17.9% vs 8.3%, p = 0.002), with most of these patients undergoing PFDD (85.7%) for their revision decompression. The mean time to revision surgery did not differ between the groups (p = 0.76). The operative characteristics and information on revision surgeries are listed in Table 4.

TABLE 4.

Operative characteristics and postdecompression surgeries

VariablePFD (n = 117)PFDD (n = 575)p Value
Mean operating room time, hrs1.98 ± 1.062.92 ± 1.32<0.0001
EBL >50 mL, n (%)12 (10.2)105 (18.3)0.04
Necessitating transfusion, n (%)0 (0)4 (0.7)>0.99
Mean length of postop hospital stay, days3.45 ± 2.584.57 ± 3.700.0001
Postop VP shunt placement, n (%)5 (4.3)39 (6.8)0.41
Postop spinal fusion, n (%)16 (13.7)68 (11.8)0.54
Revision Chiari decompression op
 1 revision decompression, n (%)21 (17.9)48 (8.3)0.002
  PFD → PFDD18
  PFD → PFD3
  PFDD → PFDD47
  PFDD → PFD1
 Multiple decompression ops, n (%)0 (0.0)4 (0.7)*>0.99
 Mean time to revision op, mos22.4 ± 17.821.0 ± 17.70.76

Mean values are presented as the mean ± SD. Boldface type indicates statistical significance.

All repeat decompressions in the multiple decompression group were PFDD.

Postoperative Signs and Symptoms

Table 5 shows the clinical outcomes for the patients’ postoperative symptoms and physical examination findings. Patients who underwent PFDD reported headache resolution or improvement significantly more often (89.6%) than those who received PFD (80.8%) (p = 0.04). PFDD was more often associated with resolved or improved back pain (86.5% vs 59.1%, p = 0.01), and patients who had experienced preoperative tremor only reported improvement postoperatively if they had undergone PFDD (PFDD 8/9 patients, PFD 0/3 patients; p = 0.02). There were no differences between the groups for the development of new postoperative signs or symptoms.

TABLE 5.

Postoperative changes in exam findings and symptoms

VariableNo. of Ptsp ValueOR*95% CI
PFDPFDD
Exam findings
 Cranial nerve
  Nystagmus95399
   None903820.590.800.27–2.85
   Resolved/improved220.174.270.30–59.35
   Stable/worse3150.780.830.15–3.04
  Dysconjugate gaze105412
   None1034100.180.250.02–3.52
   Resolved/improved100.20
   Stable/worse120.491.970.03–38.14
  Facial weakness77417
   None77416>0.99
   Resolved/improved00
   Stable/worse01>0.99
  New facial weakness00
  Hearing loss61356
   None613490.60
   Resolved/improved060.60
   Stable/worse01>0.99
  New hearing loss01>0.99
  Hoarseness51353
   None51352>0.99
   Resolved/improved01>0.99
   Stable/worse00
  New hoarseness00
  Tongue deviation95411
   None95410>0.99
   Resolved/improved00
   Stable/worse01>0.99
  New tongue deviation00
  Weak gag52323
   None51319>0.990.640.06–32.10
   Resolved/improved02>0.99
   Stable/worse120.363.150.05–61.21
  New gag weakness130.522.090.39–25.56
  Weak shrug53340
   None53340
   Resolved/improved00
   Stable/worse00
  New shrug weakness100.17
  Weak neck rotation46359
   None453550.450.510.05–25.51
   Resolved/improved140.451.970.04–20.46
   Stable/worse00
  New weak neck rotation110.318.040.10–633.20
 Spinal cord
  Upper-extremity weakness80366
   None783590.670.760.14–7.64
   Resolved/improved16>0.990.760.02–6.40
   Stable/worse110.334.620.06–363.62
  New upper-extremity weakness220.134.670.33–64.96
  Lower-extremity weakness80366
   None793600.801.320.16–61.31
   Resolved/improved03>0.99
   Stable/worse130.551.530.03–19.34
  New lower-extremity weakness02>0.99
  Light touch deficit25158
   None25158
   Resolved/improved00
   Stable/worse00
  New light touch deficit110.316.540.08–516.60
  Deep tendon reflexes84359
   Absent6160.281.650.51–4.61
   Normal632850.380.780.44–1.43
   Hypoactive7250.641.210.43–3.02
   Hyperactive8330.921.040.40–2.41
 Cerebellar
  Gait instability100454
   Normal934250.820.910.37–2.53
   Improved3200.780.670.12–2.33
   Stable/worse490.272.060.45–7.54
Symptoms
 Prior headache73346
  Resolved/improved593100.040.490.24–0.76
  Stable/worse1436
 New headache2097
  Occipital/suboccipital5140.311.980.48–6.95
  Frontal4230.700.790.18–2.81
  Holocranial11480.811.250.42–3.74
  Parietal04>0.99
  Temporal080.36
 Motor/sensory deficits
  Prior weakness1275
   Resolved/improved9580.860.880.19–5.61
   Stable/worse317
  New weakness02>0.99
  Prior sensory deficits18130
   Resolved/improved161040.372.00.42–18.95
   Stable/worse226
  New sensory deficit4280.630.690.17–2.03
 Cranial nerve
  Prior double vision421
   Resolved/improved2200.060.050.001–1.65
   Stable/worse21
  New double vision02>0.99
  Prior dysphagia1162
   Resolved/improved1157>0.99
   Stable/worse05
  New dysphagia120.432.470.04–47.73
  Prior choking730
   Resolved/improved7260.57
   Stable/worse04
  New choking100.17
  Prior sleep apnea724
   Resolved/improved4170.650.550.07–4.84
   Stable/worse37
  New sleep apnea00
 Neck & back pain
  Prior neck pain51205
   Resolved/improved431810.480.710.28–1.97
   Stable/worse824
  New neck pain318>0.990.810.15–2.86
  Prior back pain2289
   Resolved/improved13770.010.220.07–0.74
   Stable/worse912
  New back pain270.651.410.14–7.53
 Cerebellar
  Prior tremors39
   Resolved/improved080.02
   Stable/worse31
  New tremors01>0.99
  Prior balance/gait ataxia1784
   Resolved/improved13690.730.710.18–3.40
   Stable/worse415
  New balance/gait ataxia03>0.99

Boldface type indicates statistical significance.

The reference group is PFDD.

Radiological Measurements

Preoperative and postoperative radiological measurements are displayed in Table 6. Both PFD and PFDD yielded significantly smaller mean AP syrinx diameters after surgery (p < 0.0001 for both). However, when comparing percent changes in mean syrinx size between groups, patients who received PFDD had a significantly greater percent change in syrinx diameter (43.7% vs 26.9%, p = 0.0001) and syrinx length (18.9% vs 5.6%, p = 0.04) compared with those who received PFD. A significantly greater proportion of PFDD patients (37.6%) had postoperative syringes that were ≤ 2 mm in AP diameter compared with PFD patients (27.3%) (p = 0.04).

TABLE 6.

Postoperative changes in radiological measurements

VariablePFDPFDDp Value
AP syrinx diameter, mm
 Mean preop6.36 ± 2.797.75 ± 3.07<0.0001
 Mean postop4.65 ± 2.904.36 ± 3.280.34
 % change in AP diameter26.9%43.7%0.0001
 p value (preop vs postop)<0.0001<0.0001
No. of pts w/ syrinx ≤2 mm after decompression op32 (27.3%)216 (37.6%)0.04
Syrinx length (vertebral segments)
 Mean preop7.44 ± 4.439.15 ± 4.610.0002
 Mean postop7.02 ± 4.687.42 ± 4.290.39
 % change in length5.6%18.9%0.04
 p value (preop vs postop)0.48<0.0001
No. of pts w/ preoperative syringes >10 mm94360
AP syrinx diameter
 Mean preop5.37 ± 1.946.14 ± 1.880.001
 Mean postop3.36 ± 1.912.86 ± 2.000.03
 % change37.4%53.4%<0.0001
 p value (preop vs postop)<0.0001<0.0001
Syrinx length (vertebral segments)
 Mean preop6.68 ± 4.168.16 ± 4.560.003
 Mean postop6.27 ± 4.406.54 ± 4.220.59
 % change6.1%19.8%0.02
 p value (preop vs postop)0.51<0.0001
CXA, °
 Mean preop142.93 ± 14.10145.77 ± 12.810.05
 Mean postop142.47 ± 21.66142.02 ± 13.480.83
 % change0.32%2.6%0.19
 p value (preop vs postop)0.85<0.0001
pBC2, mm
 Mean preop6.71 ± 1.236.89 ± 1.260.15
 Mean postop6.56 ± 1.176.67 ± 1.210.36
 % change2.2%3.2%0.68
 p value (preop vs postop)0.340.003

Boldface type indicates statistical significance.

In an attempt to limit the effects of procedural bias related to particularly large syringes, subanalyses were performed for patients with a preoperative AP syrinx diameter < 10 mm (94 PFD patients and 360 PFDD patients; Table 6). These subanalyses demonstrated that both PFD and PFDD yielded significant decreases in mean syrinx diameter (p < 0.0001). However, the PFDD group experienced a higher percent decrease in syrinx diameter compared with the PFD group (53.4% vs 37.4%, p < 0.0001). Postoperatively, only PFDD produced a significant mean decrease in syrinx length (p < 0.0001). PFDD also yielded a significantly higher mean percent decrease in syrinx length compared with PFD (19.8% vs 6.1%, p = 0.02).

Preoperative and postoperative CXA and pBC2 were not different between the PFD and PFDD groups. However, the calculated change from preoperative to postoperative values was larger for the PFDD group (p < 0.0001 for reduction in CXA and p = 0.003 for reduction in pBC2).

Univariate and Multivariate Analyses

We conducted univariate and multivariate analyses to assess for the effect of confounding variables on complications within 6 months and found no significant affects from potential confounding variables (Table 7). Specifically, age, pBC2 distance, and syrinx diameter did not impact complication rates. After accounting for these factors, type of surgery was still significantly different, with PFDD patients having 1.5 greater odds of complications compared with PFD patients (p = 0.03). PFDD patients had 1.66 greater odds of complications compared with PFD in univariate analysis (p = 0.01).

TABLE 7.

Logistic regression results for potential factors influencing postoperative complications within 6 months

Variablep ValueOR95% CI
Univariate analysis
 Age0.101.091.05–1.18
 PFDD (vs PFD)0.011.661.15–2.38
 CXA0.540.990.98–1.01
 pBC2 distance0.091.100.98–1.22
 Frontal-occipital ratio0.652.980.03–33.42
 Syrinx diameter0.031.051.005–1.10
 Syrinx length0.281.020.98–1.05
 Preop hydrocephalus0.950.980.43–2.22
Multivariate analysis
 Age0.301.020.98–1.05
 PFDD (vs PFD)0.031.541.05–2.25
 pBC2 distance0.271.070.95–1.20
 Syrinx diameter0.071.040.98–1.09

Boldface type indicates statistical significance.

Discussion

In this study, we conducted retrospective analyses of retrospectively and prospectively collected data from the PRSRC to compare complications and outcomes between PFD and PFDD in patients with CM1-SM. This represents the first large-scale, multi-institutional study of pediatric patients undergoing PFD compared with those undergoing PFDD for CM1-SM. Our results indicated that the overall complication rate between the groups was equivalent intraoperatively and beyond 6 months after surgery. There was a higher complication rate in the PFDD group within 6 months postoperatively, especially regarding pseudomeningocele rates. Of note, pseudomeningoceles were only documented in the registry if they were both clinically significant and radiographically evident. Asymptomatic pseudomeningoceles were not included. Interestingly, there were several pseudomeningoceles and CSF leaks in the PFD group, which may represent an unintended durotomy. The PFD group did have shorter operative times, less blood loss, and shorter hospital stays, but these patients more frequently required revision surgery compared with PFDD patients. PFDD was associated with better headache and back pain improvement and more significant improvements in syrinx size and other radiographic measures. Other than headache and back pain, both groups seemed to have similar outcomes for the various postoperative signs and symptoms reported.

Our data indicating a significantly higher overall complication rate within 6 months after PFDD are in line with previously published studies. In a prior meta-analysis, Chai et al. found a higher rate of aseptic meningitis (relative risk 4.02) and CSF leak (relative risk 5.23) in the PFDD group.5 Munshi et al. found that in a group of 11 patients undergoing PFD, there was just one complication of a superficial incision infection compared with 10 of 23 patients who underwent PFDD and had some form of minor complication.6 Yeh et al. found that patients undergoing PFDD were much more likely to have complications than those who underwent PFD.9 Chotai and Medhkour found a complication rate at 2 times odds for the PFDD group compared with the PFD group,15 and Lee et al. found no complications in the PFD group compared with 19.4% in the PFDD group.16 In a study using a large national registry, Shweikeh et al. found a higher rate of complications in the PFDD group.18 We also found a higher rate of reoperation in the PFD group compared with the PFDD group. Other studies have found similar results. Mutchnick et al. found that among 64 patients who underwent PFDD, only 2 required repeat decompression compared with 7 of 56 patients in the PFD group.12 The higher reoperation rate, however, needs to be weighed against the lower complication rate.

We found that hospital stay, operative time, and blood loss were greater in the PFDD group than in the PFD group, which is perhaps not surprising given that PFDD is a more complex and invasive procedure. However, transfusion rates were similar between the groups. Yeh et al. found similar benefit in the PFD group compared with the PFDD group in hospital stay.9 Mutchnick et al. found similar reductions in operating room time and hospital stay in the PFD group,12 while Chotai and Medhkour found a shorter length of hospital stay in the PFD group.15 Lee et al. found that operating room times were roughly an hour shorter and hospital stays a day shorter in the PFD group compared with the PFDD group.16 Looking at a large national registry, Shweikeh et al. found longer hospital stays and higher charges in the PFDD group.18 Overall, it seems that PFD may be associated with a reduction in operative and hospital needs, which may portend a faster recovery and a reduction in resource utilization.

Our results demonstrated significant improvements in several radiographic parameters in the PFDD group compared with the PFD group, which is in line with previous research. However, it should be noted that the improvement in radiographic parameters seen in the PFDD group did not necessarily yield a more substantial improvement in symptoms over PFD, except for patients presenting with headaches. Additionally, our study design of a 1-year follow-up did not enable us to assess the effects of syrinx reduction on long-term spinal deformity. Using the PRSRC, Hale et al. found that younger age and PFDD were associated with greater rates of syrinx resolution.21 In a meta-analysis, Chai et al. saw a significant decrease in syrinx in the PFDD group (relative risk 1.57).5 Munshi et al. also saw similar improvement in radiographic syrinx in the PFDD group compared with the PFD group.6 Yeh et al. found similar results in a study that used intraoperative ultrasound to guide decision-making between the PFDD and PFD.9 Intraoperative ultrasound may be a useful adjunct to make a determination between these two types of surgery, but better understanding of this tool is needed in CM1-SM patients. Additionally, while radiographic parameters such as syrinx size or length may change, this was not necessarily associated with a greater clinical benefit in spine-related parameters other than back pain. Studies examining the association between syrinx reduction and improvements in symptoms or physical examination findings would help clarify the benefits that patients may experience from significantly smaller syrinxes following PFDD. Studies comparing PFDD for patients with and without SM may also help elucidate whether PFDD is particularly useful in the population of patients with a syrinx. Moreover, there were no postoperative differences between PFD and PFDD for either CXA or pBC2, and the mean pBC2 remained < 7 mm regardless of surgery type. These findings, we believe, merit further investigation in future studies.

We did find that PFDD was more likely to benefit patients with headache or back pain, which may support this more invasive approach for the elimination of these particular symptoms. However, if these symptoms are not the main focus of the presentation, then PFD may be sufficient since the outcomes for other signs and symptoms are equivalent with a lower risk of postoperative complications and decrease resource utilization.

Limitations

There are limitations to the current study. While PRSRC data have been prospectively collected for a number of patients, a large proportion of the data was collected retrospectively. Unfortunately, there are no data from the prospective cohort regarding the number of patients or legal guardians who refused to give consent for their child to be included in the PRSRC database, which could hide a bias in patient selection. The retrospective cohort was obtained using a waiver of consent, and thus enrollment could not be declined. These patients were selected and enrolled by participating study teams based on qualification criteria. While efforts were made to consecutively capture all patients meeting criteria both retrospectively and prospectively, there is a possibility of convenience sampling in the retrospective cohort. However, across the three largest centers, the patient enrollment rate was 95%. Fortunately, the prospectively and retrospectively acquired cohorts did not differ based on mean age at surgery, mean follow-up time, and sex. Additionally, this is a descriptive study that applies to pediatric patients with CM1-SM from the PRSRC database only, limiting its generalizability to CM1 patients without SM. Therefore, the results are only applicable to CM1 patients with SM. This study also only pertains to surgically treated patients and pediatric patients with CM1-SM and is limited to 1 year of follow-up. The PRSRC includes institutions with a specific interest in CM1-SM. Institutional and surgeon biases between and within centers may also contribute to the study findings. Data reporting in the database is dependent on the efforts of busy investigators or research administrators at the various institutions. While every attempt has been made to standardize data entry, there is still some variability in data collection and how data are reported. The data monitor for the study remotely reviewed data sets for the participants to minimize this variability. All data were processed with the reports available, and this possibly leads to a higher frequency of categorical outcomes, as negative findings are less likely reported than positive ones. There are additionally a high number of analyses performed, which does increase the chance of alpha error in this study. Finally, some signs and symptoms had small sample sizes, making both clinical and statistical significance testing challenging for those parameters.

Conclusions

Analyses of a large multicenter cohort of pediatric patients with CM1-SM demonstrated that patients undergoing PFD had a lower complication rate within 6 months of surgery and had shorter operative times, less blood loss, and a shorter length of hospital stay compared with those undergoing PFDD. However, PFDD was associated with better headache and syrinx outcomes as well as a reduced revision rate. The improved headache and radiographic outcomes seen with PFDD must be weighed against the reduced complication rate and resource utilization seen with PFD.

Acknowledgments

This publication was made possible through the support of Sam and Betsy Reeves, the Spears and O’Keefe families, and the many other contributors to the Park-Reeves Syringomyelia Research Consortium. Support was also provided by the Eunice Kennedy Shriver National Institute of Child Health & Human Development of the National Institutes of Health under award number U54 HD087011 to the Intellectual and Developmental Disabilities Research Center at Washington University. We furthermore appreciate the help of Timothy M. George, MD, and Sanjiv Bhatia, MD, who both contributed to this study but passed away before this manuscript was written.

Research reported in this publication was supported by the Park-Reeves Syringomyelia Research Consortium and the National Center for Advancing Translational Sciences of the National Institutes of Health under award number UL1 TR002345. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Additional funding was provided by an American Syringomyelia Alliance Project, Inc. grant.

Disclosures

Dr. Limbrick: research and educational support for non–study-related clinical or research effort from Medtronic, Inc. and Microbot Medical, Inc. Dr. Alden: honoraria from Takeda.

Author Contributions

Conception and design: Akbari, Park, Limbrick. Acquisition of data: Ackerman, Adelson, Ahmed, Albert, Aldana, Alden, Anderson, Bauer, Bethel-Anderson, Bierbrauer, Brockmeyer, Chern, Couture, Daniels, Dlouhy, Durham, Ellenbogen, Eskandari, Fuchs, Grant, Graupman, Greene, Greenfield, Gross, Guillaume, Hankinson, Heuer, Iantosca, Iskandar, Jackson, Jallo, Johnston, Kaufman, Keating, Khan, Krieger, Leonard, Maher, Mangano, McComb, McEvoy, Meehan, Menezes, Muhlbauer, O’Neill, Olavarria, Ragheb, Selden, Shah, Shimony, Smyth, Stone, Strahle, Tamber, Tuite, Tyler-Kabara, Wait, Wellons, Whitehead, Park, Limbrick. Analysis and interpretation of data: Akbari, Yahanda, Limbrick. Drafting the article: Akbari, Yahanda. Critically revising the article: Akbari, Yahanda, Anderson, Bauer, Limbrick. Reviewed submitted version of manuscript: Akbari, Ackerman, Adelson, Ahmed, Albert, Aldana, Alden, Bethel-Anderson, Bierbrauer, Brockmeyer, Chern, Couture, Daniels, Dlouhy, Durham, Ellenbogen, Eskandari, Fuchs, Grant, Graupman, Greene, Greenfield, Gross, Guillaume, Hankinson, Heuer, Iantosca, Iskandar, Jackson, Jallo, Johnston, Kaufman, Keating, Khan, Krieger, Leonard, Maher, Mangano, McComb, McEvoy, Meehan, Menezes, Muhlbauer, O’Neill, Olavarria, Ragheb, Selden, Shah, Shannon, Shimony, Smyth, Stone, Strahle, Tamber, Torner, Tuite, Tyler-Kabara, Wait, Wellons, Whitehead, Park, Limbrick. Approved the final version of the manuscript on behalf of all authors: Akbari. Statistical analysis: Akbari, Yahanda, Torner. Administrative/technical/material support: Park, Limbrick. Study supervision: Limbrick.

Supplemental Information

Previous Presentations

This work was presented as a podium talk at the 2021 AANS/CNS Section on Pediatric Neurological Surgery Annual Meeting, Salt Lake City, Utah, December 7–10, 2021.

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Illustration from Cinalli et al. (pp 119–127). Printed with permission from © CC Medical Arts.
  • 1

    Aitken LA, Lindan CE, Sidney S, et al. Chiari type I malformation in a pediatric population. Pediatr Neurol. 2009;40(6):449454.

  • 2

    Arnautovic A, Splavski B, Boop FA, Arnautovic KI. Pediatric and adult Chiari malformation Type I surgical series 1965-2013: a review of demographics, operative treatment, and outcomes. J Neurosurg Pediatr. 2015;15(2):161177.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Strahle J, Muraszko KM, Kapurch J, Bapuraj JR, Garton HJL, Maher CO. Chiari malformation Type I and syrinx in children undergoing magnetic resonance imaging. J Neurosurg Pediatr. 2011;8(2):205213.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Wu YW, Chin CT, Chan KM, Barkovich AJ, Ferriero DM. Pediatric Chiari I malformations: do clinical and radiologic features correlate?. Neurology. 1999;53(6):12711276.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Chai Z, Xue X, Fan H, et al. Efficacy of posterior fossa decompression with duraplasty for patients with Chiari malformation type I: a systematic review and meta-analysis. World Neurosurg. 2018;113:357365.e1.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Munshi I, Frim D, Stine-Reyes R, Weir BKA, Hekmatpanah J, Brown F. Effects of posterior fossa decompression with and without duraplasty on Chiari malformation-associated hydromyelia. Neurosurgery. 2000;46(6):13841390.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    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(2)(suppl):184188.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    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. 2004;20(5):349356.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

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