- Email: [email protected]
Long-Term Clinical and Radiologic Postoperative Outcomes After C1-C2 Pedicle Screw Techniques for Pediatric Atlantoaxial Rotatory Dislocation
Original Article
Long-Term Clinical and Radiologic Postoperative Outcomes After C1-C2 Pedicle Screw Techniques for Pediatric Atlantoaxial Rotatory Dislocation Xinjie Wu1,2, Yafeng Li1, Mingsheng Tan1,2, Ping Yi1, Feng Yang1, Xiangsheng Tang1, Qingying Hao1
BACKGROUND: Although C1-C2 pedicle screw techniques have been extensively reported in pediatric series, reports on their use have examined only small series with short follow-up periods. The aim of this study was to report pediatric patients with atlantoaxial rotatory dislocation treated with these techniques with a minimum 5-year follow-up.
-
METHODS: Retrospective review was performed of 27 pediatric patients with atlantoaxial rotatory dislocation who underwent C1-C2 pedicle screw fixation between 2004 and 2012. Clinical and radiographic outcomes were collected and compared with a control group.
-
RESULTS: Follow-up period was 60e142 months (mean 84 months). Torticollis was completely corrected postoperatively in all but 1 patient. All patients experienced significant pain relief and improvement in range of motion, and 6 patients with neurologic deficits experienced significant improvement postoperatively. Both atlantodental interval and space available for the cord were significantly improved compared with preoperative values. At final follow-up, curvature was lordotic in 20 cases and straight in 7 cases. Compared with the control group, range of motion of the patient group was not significantly different in any direction except in flexion and rotation. Mean anteroposterior diameters of the spinal canal at C1 and C2 levels were not significantly different from the control group.
-
CONCLUSIONS: C1-C2 pedicle screw techniques are safe and effective for treatment of atlantoaxial rotatory
-
Key words Atlantoaxial - Pediatric - Pedicle screws -
Abbreviations and Acronyms AARD: Atlantoaxial rotatory dislocation ADI: Atlantodental interval AP: Anteroposterior CT: Computed tomography ROM: Range of motion VA: Vertebral artery
e404
www.SCIENCEDIRECT.com
dislocation and result in no obvious limitation on growth in older children.
INTRODUCTION
A
lthough C1-C2 pedicle screw techniques are currently routinely performed in adult patients, the atlantoaxial complex in pediatric patients poses many unique challenges to successful screw fixation.1 In particular, immature bone, small vertebral body size, and craniovertebral anomalies represent potential limiting factors of atlantoaxial pedicle screw fixation in children.2 Although these techniques for upper cervical surgery have been extensively reported in pediatric series,3-5 the reports have described only small series with short follow-up periods. We present a study on pediatric patients with atlantoaxial rotatory dislocation (AARD) treated with C1-C2 pedicle screw techniques and a minimum 5-year follow-up period. MATERIALS AND METHODS Ethical approval for this study was obtained from the local Medical Ethics Committee. Patients Between 2004 and 2012, 27 pediatric patients with AARD who underwent C1-C2 pedicle screw fixation were treated in our hospital (a tertiary hospital). The inclusion criteria included intractable pain resistant to nonsurgical treatment, intolerance to nonsurgical treatment, instability, and progressive neurologic dysfunction. The exclusion criteria included an occipitalized atlas, an abnormal C1 posterior arch, a deficient C1 posterior arch, and
From the 1Department of Spine Surgery, China-Japan Friendship Hospital, Beijing; and 2 Graduate School of Peking Union Medical College, Beijing, China To whom correspondence should be addressed: Mingsheng Tan, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 115:e404-e421. https://doi.org/10.1016/j.wneu.2018.04.062 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Table 1. Clinical Data of Patients (N ¼ 27) Parameter Age, years, mean SD (range) Sex, male/female
Value 9.1 1.2 (5e11) 8/19
Predisposing factors Falls
9
Humerus fractures
7
Clavicle fractures
5
Upper respiratory tract infection
2
Not applicable
2
Nasopharyngeal infection
1
Neck surgery
1
Clinical symptoms Occipitocervical pain
27
Torticollis (“cock robin” position)
27
Torticollis direction, left/right
11/16
Limited range of motion
27
Neurologic deficit
6
Course of disease, months, mean SD (range)
2.6 1.3 (1.2e6)
Surgical Procedure No patients underwent emergency surgery. Neurologic function was monitored by intraoperative somatosensory evoked potentials. After endotracheal intubation and general anesthesia, the patient was placed in the prone position with the head immobilized in slight flexion using a Mayfield headholder. The patient was prepared and draped in a routine manner, and a standard midline incision was made from the inion to the C2 spinous process to expose the posterior elements of the atlas and axis. Then the C1 posterior arch was dissected approximately 14e15 mm lateral to the posterior tubercle along the posteroinferior border subperiosteally using 2 Penfield dissectors. The C2 nerve root and venous plexus were dissected caudally, and the vertebral artery (VA) was dissected rostrally. C1 pedicle screws were implanted according to our previous study.7 If the height of the C1 posterior arch at the VA groove was <4 mm, a method called the pedicle exposure technique, which we reported in a previous study, was performed.8 A high-speed burr was used to remove the approximately 3-mm-long outer narrow bone of the C1 posterior arch at the VA groove along the trajectory, and a 3.5-mm screw was safely inserted. Atlantoaxial reduction was completed by the lever system, which involved pulling C1 backward and pushing C2 downward and forward. Autologous structural and cancellous bone grafting was performed between the decorticated posterior arch and the C2 spinous process. Rigid cervical collar protection was maintained for approximately 8e12 weeks postoperatively.
Fielding’s classification Type II
3
Type III
13
Os odontoideum
11
persistent first intersegmental artery. Clinical data of patients are presented in Table 1. Preoperative Assessment Radiologic evaluations included x-ray plain films, computed tomography (CT) with three-dimensional reconstruction, and magnetic resonance imaging. Fielding classification was used to evaluate the extent of AARD on axial CT images: type I, unilateral facet subluxation with intact transverse ligament and no displacement between anterior arch of C1 and dens; type II, unilateral facet subluxation with anterior displacement of 3e5 mm; type III, bilateral anterior facet displacement with interval between C1 arch and dens >5 mm; type IV, atlas displaced posteriorly.6 Eleven patients with os odontoideum and anterior dislocation of the atlas were unable to be classified according to Fielding classification. To determine the feasibility of inserting pedicle screws, both x-rays and CT scans were used to confirm whether C1-C2 pedicle screws could be inserted. For patients with good compliance, reducibility was determined by attempted traction (maximum weight could not exceed one sixth of the patient’s weight) for 2 weeks through flexion-extension or by CT before surgery. To further confirm reducibility, patients were evaluated under general anesthesia using fluoroscopy. No irreducible cases were observed in our study.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
Evaluation Indexes The postoperative outcomes were recorded and evaluated clinically and radiologically at 1 month and 1 year after the operation and annually thereafter. The Japanese Orthopaedic Association score was used to evaluate the improvement of neurologic functions. The pain intensity was compared before and after the operation using a visual analog scale score with a scale of 0e10. For radiologic follow-up, the atlantodental interval (ADI) and the space available for the cord were recorded before and after the procedures for comparison (Figure 1). In cases with an incomplete odontoid process, the remaining attached part of the odontoid was used to measure ADI and space available for the cord. The cervical curvature was classified into 3 types and recorded during the follow-up period (Figure 2). In addition, bony fusion was assessed on CT and confirmed when bridging trabeculae were observed.9 Complete reduction was identified as ADI 5 mm, whereas partial reduction was defined as ADI of 5e7 mm.10 To determine whether growth within the construct continued after posterior fusion, 54 asymptomatic subjects matched for age and sex were selected as a radiographic control group (Part of the control group, see Supplementary Figures 1-20). We measured and compared anteroposterior (AP) diameters of the spinal canal at C1, C2, and C5 levels at the final follow-up visit. To eliminate differences owing to the magnification of the radiographs, the ratios of the AP diameter of the spinal canal at the C1 and C2 levels compared with C5 (ratio at C1 and C2 level) were determined. In addition, the cervical range of motion (ROM) was recorded for comparison with the control group at the final follow-up visit in flexion, extension, left and right lateral bending, and left and right rotation directions.
www.WORLDNEUROSURGERY.org
e405
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Figure 2. Cervical spine alignment. Lordosis, anterior displacement >2 mm; straight, anterior or posterior displacement <2 mm; kyphosis, posterior displacement 2 mm.
treatment. The patient with a superficial surgical site infection was treated with antibiotics. The mean operative time was 108.7 19.4 minutes (range, 90e130 minutes), and the mean estimated blood loss was 154.7 42.4 mL (range, 135e200 mL) (Figures 3 and 4).
Figure 1. Measurement of the atlantodental interval (a) and space available for the cord (b).
Statistical Analysis Paired t tests were used to compare changes in parametric values before and after surgery. The c2 test and Fisher exact test or the Mann-Whitney U test was employed for nonparametric comparisons. The t test, c2 test, and Mann-Whitney U test were considered significant if the P value was <0.05. Statistical analyses were performed using IBM SPSS Version 20.0 (IBM Corp., Armonk, New York, USA).
RESULTS Follow-Up and Clinical Results The follow-up period was 60e142 months (mean 84 months). No major intraoperative or postoperative complications, including neurologic injury, VA injury, or instrumentation failure, occurred in any patients. However, pneumonia and superficial surgical site infection were observed in 2 patients. The patient with pneumonia was transferred to the intensive care unit and underwent emergent tracheostomy, and the symptoms resolved after appropriate
e406
www.SCIENCEDIRECT.com
Functional Results Torticollis was completely corrected postoperatively in all but 1 patient. Although the patient still had mild symptoms of torticollis, the condition did not influence cervical ROM. All patients obtained significant pain relief and improvement in ROM, and 6 patients with neurologic deficits experienced significant improvement postoperatively (Figure 5AeC). ROM at the final follow-up visit was significantly increased compared with ROM 6 months postoperatively. Compared with the control group, ROM of the patients was not significantly different in all directions except in flexion and rotation (Figure 5F). Radiologic Results Complete reduction was confirmed in 21 patients, whereas partial reduction occurred in 6 patients. Although partial reduction was observed in 6 patients, no neurologic deterioration was observed during the entire follow-up period. All patients achieved osseous fusion with a mean duration of 4.1 0.5 months (range, 3e6 months) postoperatively. Stability was confirmed in all patients via flexion-extension on lateral cervical radiographs. No pseudoarticulation formation, recurrence of AARD, or abnormal cervical curvature was observed during the follow-up period. Both ADI and space available for the cord were significantly improved compared with preoperative values (Figure 5D and E). The cervical curvature was lordotic in 24 cases and straight in 3 cases before surgery.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Figure 3. A 5-year-old boy with os odontoideum and atlantoaxial rotatory dislocation. (A) Preoperative sagittal computed tomography showing a decrease in space available for the cord. (B) Preoperative three-dimensional computed tomography. (C) Preoperative magnetic resonance imaging showing spinal cord compression. (D) Lateral x-ray showing perfect reduction and normal space available for the cord postoperatively. (E) Sagittal
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
computed tomography showing osseous fusion after 5 months. (F and G) Flexion-extension x-ray showing atlantoaxial stability and no hardware failure 9 years postoperatively. (H) Magnetic resonance imaging showing normal diameter of the spinal canal. (I) Complete correction of torticollis 9 years postoperatively. (J) Range of motion for right and left rotation 9 years postoperatively.
www.WORLDNEUROSURGERY.org
e407
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Figure 4. An 8-year-old girl with transverse ligament disruption and atlantoaxial rotatory dislocation. (AeC) Preoperative computed tomography and three-dimensional reconstruction showing atlantoaxial rotatory dislocation, enlarged atlantodental interval, and decreased space available for the cord. (D) Lateral x-ray showing perfect reduction and normal atlantodental interval postoperatively. (E) Sagittal computed tomography
e408
www.SCIENCEDIRECT.com
showing osseous fusion 10 years postoperatively. (F) Magnetic resonance imaging showing normal diameter of the spinal canal. (G and H) Flexion-extension radiographs showing atlantoaxial reduction and cervical range of motion 10 years after the operation. (I) Mild limited range of motion in right and left rotation at 6 months postoperatively. (J) Improved range of motion of right and left rotation at 10 years postoperatively.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Figure 5. Functional results. (AeE) *P < 0.05 compared with preoperative data; **P < 0.05 compared with data obtained 6 months postoperatively. (F) *P < 0.05 compared with the control group at the final follow-up visit. (G and H) Compared with the control group, no significant differences were observed between the 2 groups in anteroposterior diameters at the C1 and C2
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
levels and ratio at C1 and C2 level. JOA, Japanese Orthopaedic Association; VAS, visual analog scale; RLB, right lateral bending; LLB, left lateral bending; RR, right rotation; LR, left rotation; ADI, atlantodental interval; SAC, space available for the cord; ROM, range of motion; AP, anteroposterior.
www.WORLDNEUROSURGERY.org
e409
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Postoperatively, lordosis remained in 22 cases, and the cervical curvature became straight in 2 cases after 6 months. At the final follow-up visit, the curvature was lordotic in 20 cases and straight in 7 cases. During the entire follow-up period, no kyphosis or crankshaft phenomenon was observed.11 To examine growth within the construct after fusion, healthy individuals matched for age and sex were designated as a control group. No demographic difference was observed between the 2 groups. Mean AP diameter of the spinal canal at the C5 level was 18.1 1.4 mm at the final follow-up visit, which did not differ significantly from the control group (18.7 1.9 mm) (P ¼ 0.15). Mean AP diameters of the spinal canal at the C1 and C2 levels were not significantly different from the control group. Similarly, mean ratio at C1 and C2 level in the patient group did not differ significantly from the control group (Figure 5G and H).
DISCUSSION AARD occurs primarily in pediatric patients, presumably because of ligamentous laxity, a shallower and more horizontally oriented joint surface in the atlantoaxial joint, incompletely developed neck muscles, and a relatively larger head.12 Furthermore, AARD is usually preceded by infection or trauma.13,14 In our study, 24 patients (89%) had a history of trauma or infection. These predisposing factors were also common in previous studies.15-17 In addition, 1 patient presented with torticollis after neck surgery. Hence, surgeons should be aware that AARD may occur after head and neck surgery in pediatric patients.18,19 Some patients may develop AARD without any obvious predisposing factors, such as 2 patients in our study. The clinical picture of AARD includes torticollis, occipitocervical pain, and limited ROM. Infection, surgery, or minor trauma can cause painful contractions of the neck muscles and result in a self-protective posture to relieve pain, which initiates torticollis. The patient’s head is held in a well-described “cock robin” position, in which the neck is laterally flexed to 1 side, and the chin is turned to the other side.20 In this study, neurologic deficits were observed in 22% of cases. This result could be explained by the fact that the C1 and C2 levels are relatively larger than the counterpart levels in the subaxial cervical spine. No irreducible dislocations were observed in our study. The reasons for this may be that the course of the disease was relatively short (i.e., approximately 2.6 months), and the remodeling process of the atlantoaxial joint was not obvious. In addition, reducibility determined by flexion-extension radiographs without anesthesia is unreliable because the result may be affected by the neck muscles. Hence, assessment under anesthesia is mandatory. AARD can be a particularly difficult problem to manage in pediatric patients. Conservative treatment includes rigid cervical orthosis, traction, and a halo brace for a prolonged duration, which are cumbersome to patients. Ishii et al.21 reported a novel remodeling therapy for external fixation to preserve atlantoaxial joint movement. However, halo fixation (mean 2.4 months) is still required after successful closed manipulation.22 In our experience, prolonged traction, which keeps a pediatric patient bedridden for several weeks, is unacceptable. In addition, the compliance associated with a halo brace in children is poor, and
e410
www.SCIENCEDIRECT.com
the overall complication rate is 53%. Complications include pin loosening, infection, nerve injury, and pressure sores.23,24 Fielding and Hawkins6 recommended that patients with symptoms lasting >3 months should undergo fusion, given the high likelihood of recurrence. Therefore, atlantoaxial reduction and fusion were performed in all cases. Short-segment fixation is the optimal strategy for AARD. Several studies have reported the use of C1 lateral mass screws for atlantoaxial fixation in pediatric patients.1,25 However, this technique increases the risk of intraoperative bleeding from the venous plexus and C2 nerve root irritation owing to the deep operative area.19 Hence, given the possible neurologic damage and low blood volume of pediatric patients, use of the C1 pedicle screw technique with a high entry point is more secure. In the present study, we analyzed the cervical ROM of 27 pediatric patients undergoing C1-C2 pedicle screw fixation. The preoperative ROM was decreased owing to pain, stiffness, muscle spasm, and even a self-protective decrease in ROM to prevent further spinal cord injury. The 6-month postoperative ROM increased in the flexion and extension directions, perhaps because cervical pain and stiffness were ameliorated after achieving atlantoaxial stability. However, the 6-month postoperative ROM of rotation was significantly lower than the preoperative value. This can be attributed to the loss of atlantoaxial ROM in axial rotation. Our previous study showed that the atlantoaxial ROM was approximately 40 in rotation and only 5 in lateral bending.26 Hence, the ROM in the lateral bending direction was only slightly affected postoperatively. The ROM in all directions at the final follow-up visit was significantly increased compared with the preoperative and 6-month postoperative values. Increased cervical ROM may be induced by subaxial compensation for the loss of atlantoaxial motion. Previous studies found increased or decreased compensation after atlantoaxial or occipitocervical fusion via remodeling of the subaxial intervertebral joints or increased ligamentous laxity.26,27 Ishikawa et al.28 found significantly smaller C1, C2, and ratio at C1 level values after posterior fusion using a wiring technique. They also found 6 (75%) patients with malalignment at final the follow-up visit; however, the study consisted of only 8 pediatric patients. In another study, Kanna et al.29 reported that pedicle screws had no impact on spinal growth or cervical canal dimensions in pediatric patients. According to previous studies, the craniovertebral region in children may reach adult size and configuration by approximately 8e10 years of age.4,30,31 According to Ogden,32 the size of the spinal canal at the atlas nearly reaches its maximum at 4e6 years of age. In our study, the mean age of patients was 9.1 years, which may have led to the lack of difference from the control group. Hence, we speculate that the potential of C1-C2 pedicle screw techniques for growth limitation was minimal. Furthermore, the rate of malalignment in our study was 26%, and crankshaft phenomenon was not observed at the final follow-up visit, which may be attributed to the short-segment and rigid fixation of C1-C2 pedicle screw techniques. Gluf and Brockmeyer33 reported that the C1-C2 transarticular screw technique did not result in growth deformity in the sagittal or coronal plane. Our study has several limitations. First, the sample size is small because AARD requiring surgery in pediatric patients is rare.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Second, it is a retrospective study. Despite its limitations, we believe that this study successfully assessed long-term outcomes (minimum 5 years) after application of C1-C2 pedicle screw techniques to treat pediatric AARD.
REFERENCES 1. Desai R, Stevenson CB, Crawford AH, Durrani AA, Mangano FT. C-1 lateral mass screw fixation in children with atlantoaxial instability: case series and technical report. J Spinal Disord Tech. 2010;23:474-479. 2. Menezes AH. Craniocervical fusions in children. J Neurosurg Pediatr. 2012;9:573-585. 3. Chen ZD, Wu J, Lu CW, Zeng WR, Huang ZZ, Lin B. C1eC2 pedicle screw fixation for pediatric atlantoaxial dislocation [e-pub ahead of print]. J Pediatr Orthop. 2017. https://doi.org/10.1097/ BPO.0000000000001111. 4. Guo X, Xie N, Lu X, Guo Q, Deng Y, Ni B. Onestep reduction and fixation applying transposterior arch lateral mass screw of C1 combined with pedicle screw of C2 and rod system for pediatric acute atlantoaxial rotatory subluxation with injury of transverse ligament. Spine (Phila Pa 1976). 2015;40:E272-E278. 5. Zhang YH, Shao J, Chou D, Wu JF, Song J, Zhang J. C1-C2 pedicle screw fixation for atlantoaxial dislocation in pediatric patients younger than 5 years: a case series of 15 patients. World Neurosurg. 2017;108:498-505. 6. Fielding JW, Hawkins RJ. Atlanto-axial rotatory fixation. (Fixed rotatory subluxation of the atlanto-axial joint). J Bone Joint Surg Am. 1977;59: 37-44. 7. Tan M, Wang H, Wang Y, Zhang G, Yi P, Li Z, et al. Morphometric evaluation of screw fixation in atlas via posterior arch and lateral mass. Spine (Phila Pa 1976). 2003;28:888-895. 8. Yi P, Dong L, Tan M, Wang W, Tang X, Yang F, et al. Clinical application of a revised screw technique via the C1 posterior arch and lateral mass in the pediatric population. Pediatr Neurosurg. 2013;49:159-165. 9. Buchowski JM, Liu G, Bunmaprasert T, Rose PS, Riew KD. Anterior cervical fusion assessment: surgical exploration versus radiographic evaluation. Spine (Phila Pa 1976). 2008;33:1185-1191. 10. Ma H, Dong L, Liu C, Yi P, Yang F, Tang X, et al. Modified technique of transoral release in onestage anterior release and posterior reduction for irreducible atlantoaxial dislocation. J Orthop Sci. 2016;21:7-12. 11. Rodgers WB, Coran DL, Kharrazi FD, Hall JE, Emans JB. Increasing lordosis of the occipitocervical junction after arthrodesis in young children: the occipitocervical crankshaft phenomenon. J Pediatr Orthop. 1997;17:762-765. 12. Goel A, Shah A. Atlantoaxial facet locking: treatment by facet manipulation and fixation. Experience in 14 cases. J Neurosurg Spine. 2011;14:3-9.
CONCLUSIONS C1-C2 pedicle screw techniques are safe and effective for the treatment of AARD and result in no obvious limitation on growth in older children.
13. Neal KM, Mohamed AS. Atlantoaxial rotatory subluxation in children. J Am Acad Orthop Surg. 2015;23:382-392. 14. Ishii K, Chiba K, Maruiwa H, Nakamura M, Matsumoto M, Toyama Y. Pathognomonic radiological signs for predicting prognosis in patients with chronic atlantoaxial rotatory fixation. J Neurosurg Spine. 2006;5:385-391. 15. Chechik O, Wientroub S, Danino B, Lebel DE, Ovadia D. Successful conservative treatment for neglected rotatory atlantoaxial dislocation. J Pediatr Orthop. 2013;33:389-392. 16. Hicazi A, Acaroglu E, Alanay A, Yazici M, Surat A. Atlantoaxial rotatory fixation-subluxation revisited: a computed tomographic analysis of acute torticollis in pediatric patients. Spine (Phila Pa 1976). 2002;27:2771-2775. 17. Wang S, Yan M, Passias PG, Wang C. Atlantoaxial rotatory fixed dislocation. Spine (Phila Pa 1976). 2016;41:E725-E732. 18. Deichmueller CM, Welkoborsky HJ. Grisel’s syndrome—a rare complication following “small” operations and infections in the ENT region. Eur Arch Otorhinolaryngol. 2010;267:1467-1473. 19. Tauchi R, Imagama S, Ito Z, Ando K, Muramoto A, Matsui H, et al. Surgical treatment for chronic atlantoaxial rotatory fixation in children. J Pediatr Orthop B. 2013;22:404-408. 20. Pang D, Li V. Atlantoaxial rotatory fixation: part 2— new diagnostic paradigm and a new classification based on motion analysis using computed tomographic imaging. Neurosurgery. 2005;57:941-953. 21. Ishii K, Matsumoto M, Momoshima S, Watanabe K, Tsuji T, Takaishi H, et al. Remodeling of C2 facet deformity prevents recurrent subluxation in patients with chronic atlantoaxial rotatory fixation: a novel strategy for treatment of chronic atlantoaxial rotatory fixation. Spine (Phila Pa 1976). 2011;36:E256-E262. 22. Matsumoto Y, Mizutani J, Suzuki N, Otsuka S, Hayakawa K, Fukuoka M, et al. Temporary internal fixation using C1 lateral mass screw and C2 pedicle screw (Goel-Harms technique) without bone grafting for chronic atlantoaxial rotatory fixation. World Neurosurg. 2017;102:696.e1-696.e6. 23. Kato G, Kawaguchi K, Tsukamoto N, Komiyama K, Mizuta K, Onohara T, et al. Recurrent dislocations of the atlantooccipital and atlantoaxial joints in a halo vest fixator are resolved by backrest elevation in an elevation angle-dependent manner. Spine J. 2015;15:e69-e74. 24. Limpaphayom N, Skaggs DL, McComb G, Krieger M, Tolo VT. Complications of halo use in children. Spine (Phila Pa 1976). 2009;34:779-784. 25. Aryan HE, Newman CB, Nottmeier EW, Acosta FL, Wang VY, Ames CP. Stabilization of
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
the atlantoaxial complex via C-1 lateral mass and C-2 pedicle screw fixation in a multicenter clinical experience in 102 patients: modification of the Harms and Goel techniques. J Neurosurg Spine. 2008;8:222-229. 26. Yang F, Dong L, Tan M, Ma H, Yi P, Tang X. In vivo analysis of cervical range of motion after revised C1-C2 pedicle screw technique for pediatric atlantoaxial instability. Pediatr Neurosurg. 2014;49:282-286. 27. Wills BP, Jencikova-Celerin L, Dormans JP. Cervical spine range of motion in children with posterior occipitocervical arthrodesis. J Pediatr Orthop. 2006;26:753-757. 28. Ishikawa M, Matsumoto M, Chiba K, Toyama Y, Kobayashi K. Long-term impact of atlantoaxial arthrodesis on the pediatric cervical spine. J Orthop Sci. 2009;14:274-278. 29. Kanna PR, Shetty AP, Rajasekaran S. Anatomical feasibility of pediatric cervical pedicle screw insertion by computed tomographic morphometric evaluation of 376 pediatric cervical pedicles. Spine (Phila Pa 1976). 2011;36:1297-1304. 30. Anderson RC, Ragel BT, Mocco J, Bohman L-E, Brockmeyer DL. Selection of a rigid internal fixation construct for stabilization at the craniovertebral junction in pediatric patients. J Neurosurg. 2007;107(1 suppl):36-42. 31. Galindo MJ, Francis WR. Atlantal fracture in a child through congenital anterior and posterior arch defects. A case report. Clin Orthop Relat Res. 1983;178:220-222. 32. Ogden JA. Radiology of postnatal skeletal development. XI. The first cervical vertebra. Skeletal Radiol. 1984;12:12-20. 33. Gluf WM, Brockmeyer DL. Atlantoaxial transarticular screw fixation: a review of surgical indications, fusion rate, complications, and lessons learned in 67 pediatric patients. J Neurosurg Spine. 2005;2:164-169. Conflict of interest statement: This work was supported by grants from Capital Characteristic Clinical project of Beijing Municipal Science and Technology Commission (http://www. bjkw.gov.cn/n8785584/index.html) (Grant No. Z161100000516009). No individuals employed or contracted by the funders played any role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Received 20 February 2018; accepted 9 April 2018 Citation: World Neurosurg. (2018) 115:e404-e421. https://doi.org/10.1016/j.wneu.2018.04.062 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
e411
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
SUPPLEMENTARY DATA
Supplementary Figure 2. Part of the control group, case 2.
Supplementary Figure 1. Part of the control group, case 1.
e412
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 3. Part of the control group, case 3.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 4. Part of the control group, case 4.
www.WORLDNEUROSURGERY.org
e413
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 5. Part of the control group, case 5.
e414
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 6. Part of the control group, case 6.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 7. Part of the control group, case 7.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 8. Part of the control group, case 8.
www.WORLDNEUROSURGERY.org
e415
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 9. Part of the control group, case 9.
e416
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 10. Part of the control group, case 10.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 11. Part of the control group, case 11.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 12. Part of the control group, case 12.
www.WORLDNEUROSURGERY.org
e417
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 13. Part of the control group, case 13.
e418
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 14. Part of the control group, case 14.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 15. Part of the control group, case 15.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 16. Part of the control group, case 16.
www.WORLDNEUROSURGERY.org
e419
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 17. Part of the control group, case 17.
e420
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 18. Part of the control group, case 18.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 19. Part of the control group, case 19.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 20. Part of the control group, case 20.
www.WORLDNEUROSURGERY.org
e421
Long-Term Clinical and Radiologic Postoperative Outcomes After C1-C2 Pedicle Screw Techniques for Pediatric Atlantoaxial Rotatory Dislocation Xinjie Wu1,2, Yafeng Li1, Mingsheng Tan1,2, Ping Yi1, Feng Yang1, Xiangsheng Tang1, Qingying Hao1
BACKGROUND: Although C1-C2 pedicle screw techniques have been extensively reported in pediatric series, reports on their use have examined only small series with short follow-up periods. The aim of this study was to report pediatric patients with atlantoaxial rotatory dislocation treated with these techniques with a minimum 5-year follow-up.
-
METHODS: Retrospective review was performed of 27 pediatric patients with atlantoaxial rotatory dislocation who underwent C1-C2 pedicle screw fixation between 2004 and 2012. Clinical and radiographic outcomes were collected and compared with a control group.
-
RESULTS: Follow-up period was 60e142 months (mean 84 months). Torticollis was completely corrected postoperatively in all but 1 patient. All patients experienced significant pain relief and improvement in range of motion, and 6 patients with neurologic deficits experienced significant improvement postoperatively. Both atlantodental interval and space available for the cord were significantly improved compared with preoperative values. At final follow-up, curvature was lordotic in 20 cases and straight in 7 cases. Compared with the control group, range of motion of the patient group was not significantly different in any direction except in flexion and rotation. Mean anteroposterior diameters of the spinal canal at C1 and C2 levels were not significantly different from the control group.
-
CONCLUSIONS: C1-C2 pedicle screw techniques are safe and effective for treatment of atlantoaxial rotatory
-
Key words Atlantoaxial - Pediatric - Pedicle screws -
Abbreviations and Acronyms AARD: Atlantoaxial rotatory dislocation ADI: Atlantodental interval AP: Anteroposterior CT: Computed tomography ROM: Range of motion VA: Vertebral artery
e404
www.SCIENCEDIRECT.com
dislocation and result in no obvious limitation on growth in older children.
INTRODUCTION
A
lthough C1-C2 pedicle screw techniques are currently routinely performed in adult patients, the atlantoaxial complex in pediatric patients poses many unique challenges to successful screw fixation.1 In particular, immature bone, small vertebral body size, and craniovertebral anomalies represent potential limiting factors of atlantoaxial pedicle screw fixation in children.2 Although these techniques for upper cervical surgery have been extensively reported in pediatric series,3-5 the reports have described only small series with short follow-up periods. We present a study on pediatric patients with atlantoaxial rotatory dislocation (AARD) treated with C1-C2 pedicle screw techniques and a minimum 5-year follow-up period. MATERIALS AND METHODS Ethical approval for this study was obtained from the local Medical Ethics Committee. Patients Between 2004 and 2012, 27 pediatric patients with AARD who underwent C1-C2 pedicle screw fixation were treated in our hospital (a tertiary hospital). The inclusion criteria included intractable pain resistant to nonsurgical treatment, intolerance to nonsurgical treatment, instability, and progressive neurologic dysfunction. The exclusion criteria included an occipitalized atlas, an abnormal C1 posterior arch, a deficient C1 posterior arch, and
From the 1Department of Spine Surgery, China-Japan Friendship Hospital, Beijing; and 2 Graduate School of Peking Union Medical College, Beijing, China To whom correspondence should be addressed: Mingsheng Tan, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 115:e404-e421. https://doi.org/10.1016/j.wneu.2018.04.062 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Table 1. Clinical Data of Patients (N ¼ 27) Parameter Age, years, mean SD (range) Sex, male/female
Value 9.1 1.2 (5e11) 8/19
Predisposing factors Falls
9
Humerus fractures
7
Clavicle fractures
5
Upper respiratory tract infection
2
Not applicable
2
Nasopharyngeal infection
1
Neck surgery
1
Clinical symptoms Occipitocervical pain
27
Torticollis (“cock robin” position)
27
Torticollis direction, left/right
11/16
Limited range of motion
27
Neurologic deficit
6
Course of disease, months, mean SD (range)
2.6 1.3 (1.2e6)
Surgical Procedure No patients underwent emergency surgery. Neurologic function was monitored by intraoperative somatosensory evoked potentials. After endotracheal intubation and general anesthesia, the patient was placed in the prone position with the head immobilized in slight flexion using a Mayfield headholder. The patient was prepared and draped in a routine manner, and a standard midline incision was made from the inion to the C2 spinous process to expose the posterior elements of the atlas and axis. Then the C1 posterior arch was dissected approximately 14e15 mm lateral to the posterior tubercle along the posteroinferior border subperiosteally using 2 Penfield dissectors. The C2 nerve root and venous plexus were dissected caudally, and the vertebral artery (VA) was dissected rostrally. C1 pedicle screws were implanted according to our previous study.7 If the height of the C1 posterior arch at the VA groove was <4 mm, a method called the pedicle exposure technique, which we reported in a previous study, was performed.8 A high-speed burr was used to remove the approximately 3-mm-long outer narrow bone of the C1 posterior arch at the VA groove along the trajectory, and a 3.5-mm screw was safely inserted. Atlantoaxial reduction was completed by the lever system, which involved pulling C1 backward and pushing C2 downward and forward. Autologous structural and cancellous bone grafting was performed between the decorticated posterior arch and the C2 spinous process. Rigid cervical collar protection was maintained for approximately 8e12 weeks postoperatively.
Fielding’s classification Type II
3
Type III
13
Os odontoideum
11
persistent first intersegmental artery. Clinical data of patients are presented in Table 1. Preoperative Assessment Radiologic evaluations included x-ray plain films, computed tomography (CT) with three-dimensional reconstruction, and magnetic resonance imaging. Fielding classification was used to evaluate the extent of AARD on axial CT images: type I, unilateral facet subluxation with intact transverse ligament and no displacement between anterior arch of C1 and dens; type II, unilateral facet subluxation with anterior displacement of 3e5 mm; type III, bilateral anterior facet displacement with interval between C1 arch and dens >5 mm; type IV, atlas displaced posteriorly.6 Eleven patients with os odontoideum and anterior dislocation of the atlas were unable to be classified according to Fielding classification. To determine the feasibility of inserting pedicle screws, both x-rays and CT scans were used to confirm whether C1-C2 pedicle screws could be inserted. For patients with good compliance, reducibility was determined by attempted traction (maximum weight could not exceed one sixth of the patient’s weight) for 2 weeks through flexion-extension or by CT before surgery. To further confirm reducibility, patients were evaluated under general anesthesia using fluoroscopy. No irreducible cases were observed in our study.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
Evaluation Indexes The postoperative outcomes were recorded and evaluated clinically and radiologically at 1 month and 1 year after the operation and annually thereafter. The Japanese Orthopaedic Association score was used to evaluate the improvement of neurologic functions. The pain intensity was compared before and after the operation using a visual analog scale score with a scale of 0e10. For radiologic follow-up, the atlantodental interval (ADI) and the space available for the cord were recorded before and after the procedures for comparison (Figure 1). In cases with an incomplete odontoid process, the remaining attached part of the odontoid was used to measure ADI and space available for the cord. The cervical curvature was classified into 3 types and recorded during the follow-up period (Figure 2). In addition, bony fusion was assessed on CT and confirmed when bridging trabeculae were observed.9 Complete reduction was identified as ADI 5 mm, whereas partial reduction was defined as ADI of 5e7 mm.10 To determine whether growth within the construct continued after posterior fusion, 54 asymptomatic subjects matched for age and sex were selected as a radiographic control group (Part of the control group, see Supplementary Figures 1-20). We measured and compared anteroposterior (AP) diameters of the spinal canal at C1, C2, and C5 levels at the final follow-up visit. To eliminate differences owing to the magnification of the radiographs, the ratios of the AP diameter of the spinal canal at the C1 and C2 levels compared with C5 (ratio at C1 and C2 level) were determined. In addition, the cervical range of motion (ROM) was recorded for comparison with the control group at the final follow-up visit in flexion, extension, left and right lateral bending, and left and right rotation directions.
www.WORLDNEUROSURGERY.org
e405
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Figure 2. Cervical spine alignment. Lordosis, anterior displacement >2 mm; straight, anterior or posterior displacement <2 mm; kyphosis, posterior displacement 2 mm.
treatment. The patient with a superficial surgical site infection was treated with antibiotics. The mean operative time was 108.7 19.4 minutes (range, 90e130 minutes), and the mean estimated blood loss was 154.7 42.4 mL (range, 135e200 mL) (Figures 3 and 4).
Figure 1. Measurement of the atlantodental interval (a) and space available for the cord (b).
Statistical Analysis Paired t tests were used to compare changes in parametric values before and after surgery. The c2 test and Fisher exact test or the Mann-Whitney U test was employed for nonparametric comparisons. The t test, c2 test, and Mann-Whitney U test were considered significant if the P value was <0.05. Statistical analyses were performed using IBM SPSS Version 20.0 (IBM Corp., Armonk, New York, USA).
RESULTS Follow-Up and Clinical Results The follow-up period was 60e142 months (mean 84 months). No major intraoperative or postoperative complications, including neurologic injury, VA injury, or instrumentation failure, occurred in any patients. However, pneumonia and superficial surgical site infection were observed in 2 patients. The patient with pneumonia was transferred to the intensive care unit and underwent emergent tracheostomy, and the symptoms resolved after appropriate
e406
www.SCIENCEDIRECT.com
Functional Results Torticollis was completely corrected postoperatively in all but 1 patient. Although the patient still had mild symptoms of torticollis, the condition did not influence cervical ROM. All patients obtained significant pain relief and improvement in ROM, and 6 patients with neurologic deficits experienced significant improvement postoperatively (Figure 5AeC). ROM at the final follow-up visit was significantly increased compared with ROM 6 months postoperatively. Compared with the control group, ROM of the patients was not significantly different in all directions except in flexion and rotation (Figure 5F). Radiologic Results Complete reduction was confirmed in 21 patients, whereas partial reduction occurred in 6 patients. Although partial reduction was observed in 6 patients, no neurologic deterioration was observed during the entire follow-up period. All patients achieved osseous fusion with a mean duration of 4.1 0.5 months (range, 3e6 months) postoperatively. Stability was confirmed in all patients via flexion-extension on lateral cervical radiographs. No pseudoarticulation formation, recurrence of AARD, or abnormal cervical curvature was observed during the follow-up period. Both ADI and space available for the cord were significantly improved compared with preoperative values (Figure 5D and E). The cervical curvature was lordotic in 24 cases and straight in 3 cases before surgery.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Figure 3. A 5-year-old boy with os odontoideum and atlantoaxial rotatory dislocation. (A) Preoperative sagittal computed tomography showing a decrease in space available for the cord. (B) Preoperative three-dimensional computed tomography. (C) Preoperative magnetic resonance imaging showing spinal cord compression. (D) Lateral x-ray showing perfect reduction and normal space available for the cord postoperatively. (E) Sagittal
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
computed tomography showing osseous fusion after 5 months. (F and G) Flexion-extension x-ray showing atlantoaxial stability and no hardware failure 9 years postoperatively. (H) Magnetic resonance imaging showing normal diameter of the spinal canal. (I) Complete correction of torticollis 9 years postoperatively. (J) Range of motion for right and left rotation 9 years postoperatively.
www.WORLDNEUROSURGERY.org
e407
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Figure 4. An 8-year-old girl with transverse ligament disruption and atlantoaxial rotatory dislocation. (AeC) Preoperative computed tomography and three-dimensional reconstruction showing atlantoaxial rotatory dislocation, enlarged atlantodental interval, and decreased space available for the cord. (D) Lateral x-ray showing perfect reduction and normal atlantodental interval postoperatively. (E) Sagittal computed tomography
e408
www.SCIENCEDIRECT.com
showing osseous fusion 10 years postoperatively. (F) Magnetic resonance imaging showing normal diameter of the spinal canal. (G and H) Flexion-extension radiographs showing atlantoaxial reduction and cervical range of motion 10 years after the operation. (I) Mild limited range of motion in right and left rotation at 6 months postoperatively. (J) Improved range of motion of right and left rotation at 10 years postoperatively.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Figure 5. Functional results. (AeE) *P < 0.05 compared with preoperative data; **P < 0.05 compared with data obtained 6 months postoperatively. (F) *P < 0.05 compared with the control group at the final follow-up visit. (G and H) Compared with the control group, no significant differences were observed between the 2 groups in anteroposterior diameters at the C1 and C2
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
levels and ratio at C1 and C2 level. JOA, Japanese Orthopaedic Association; VAS, visual analog scale; RLB, right lateral bending; LLB, left lateral bending; RR, right rotation; LR, left rotation; ADI, atlantodental interval; SAC, space available for the cord; ROM, range of motion; AP, anteroposterior.
www.WORLDNEUROSURGERY.org
e409
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Postoperatively, lordosis remained in 22 cases, and the cervical curvature became straight in 2 cases after 6 months. At the final follow-up visit, the curvature was lordotic in 20 cases and straight in 7 cases. During the entire follow-up period, no kyphosis or crankshaft phenomenon was observed.11 To examine growth within the construct after fusion, healthy individuals matched for age and sex were designated as a control group. No demographic difference was observed between the 2 groups. Mean AP diameter of the spinal canal at the C5 level was 18.1 1.4 mm at the final follow-up visit, which did not differ significantly from the control group (18.7 1.9 mm) (P ¼ 0.15). Mean AP diameters of the spinal canal at the C1 and C2 levels were not significantly different from the control group. Similarly, mean ratio at C1 and C2 level in the patient group did not differ significantly from the control group (Figure 5G and H).
DISCUSSION AARD occurs primarily in pediatric patients, presumably because of ligamentous laxity, a shallower and more horizontally oriented joint surface in the atlantoaxial joint, incompletely developed neck muscles, and a relatively larger head.12 Furthermore, AARD is usually preceded by infection or trauma.13,14 In our study, 24 patients (89%) had a history of trauma or infection. These predisposing factors were also common in previous studies.15-17 In addition, 1 patient presented with torticollis after neck surgery. Hence, surgeons should be aware that AARD may occur after head and neck surgery in pediatric patients.18,19 Some patients may develop AARD without any obvious predisposing factors, such as 2 patients in our study. The clinical picture of AARD includes torticollis, occipitocervical pain, and limited ROM. Infection, surgery, or minor trauma can cause painful contractions of the neck muscles and result in a self-protective posture to relieve pain, which initiates torticollis. The patient’s head is held in a well-described “cock robin” position, in which the neck is laterally flexed to 1 side, and the chin is turned to the other side.20 In this study, neurologic deficits were observed in 22% of cases. This result could be explained by the fact that the C1 and C2 levels are relatively larger than the counterpart levels in the subaxial cervical spine. No irreducible dislocations were observed in our study. The reasons for this may be that the course of the disease was relatively short (i.e., approximately 2.6 months), and the remodeling process of the atlantoaxial joint was not obvious. In addition, reducibility determined by flexion-extension radiographs without anesthesia is unreliable because the result may be affected by the neck muscles. Hence, assessment under anesthesia is mandatory. AARD can be a particularly difficult problem to manage in pediatric patients. Conservative treatment includes rigid cervical orthosis, traction, and a halo brace for a prolonged duration, which are cumbersome to patients. Ishii et al.21 reported a novel remodeling therapy for external fixation to preserve atlantoaxial joint movement. However, halo fixation (mean 2.4 months) is still required after successful closed manipulation.22 In our experience, prolonged traction, which keeps a pediatric patient bedridden for several weeks, is unacceptable. In addition, the compliance associated with a halo brace in children is poor, and
e410
www.SCIENCEDIRECT.com
the overall complication rate is 53%. Complications include pin loosening, infection, nerve injury, and pressure sores.23,24 Fielding and Hawkins6 recommended that patients with symptoms lasting >3 months should undergo fusion, given the high likelihood of recurrence. Therefore, atlantoaxial reduction and fusion were performed in all cases. Short-segment fixation is the optimal strategy for AARD. Several studies have reported the use of C1 lateral mass screws for atlantoaxial fixation in pediatric patients.1,25 However, this technique increases the risk of intraoperative bleeding from the venous plexus and C2 nerve root irritation owing to the deep operative area.19 Hence, given the possible neurologic damage and low blood volume of pediatric patients, use of the C1 pedicle screw technique with a high entry point is more secure. In the present study, we analyzed the cervical ROM of 27 pediatric patients undergoing C1-C2 pedicle screw fixation. The preoperative ROM was decreased owing to pain, stiffness, muscle spasm, and even a self-protective decrease in ROM to prevent further spinal cord injury. The 6-month postoperative ROM increased in the flexion and extension directions, perhaps because cervical pain and stiffness were ameliorated after achieving atlantoaxial stability. However, the 6-month postoperative ROM of rotation was significantly lower than the preoperative value. This can be attributed to the loss of atlantoaxial ROM in axial rotation. Our previous study showed that the atlantoaxial ROM was approximately 40 in rotation and only 5 in lateral bending.26 Hence, the ROM in the lateral bending direction was only slightly affected postoperatively. The ROM in all directions at the final follow-up visit was significantly increased compared with the preoperative and 6-month postoperative values. Increased cervical ROM may be induced by subaxial compensation for the loss of atlantoaxial motion. Previous studies found increased or decreased compensation after atlantoaxial or occipitocervical fusion via remodeling of the subaxial intervertebral joints or increased ligamentous laxity.26,27 Ishikawa et al.28 found significantly smaller C1, C2, and ratio at C1 level values after posterior fusion using a wiring technique. They also found 6 (75%) patients with malalignment at final the follow-up visit; however, the study consisted of only 8 pediatric patients. In another study, Kanna et al.29 reported that pedicle screws had no impact on spinal growth or cervical canal dimensions in pediatric patients. According to previous studies, the craniovertebral region in children may reach adult size and configuration by approximately 8e10 years of age.4,30,31 According to Ogden,32 the size of the spinal canal at the atlas nearly reaches its maximum at 4e6 years of age. In our study, the mean age of patients was 9.1 years, which may have led to the lack of difference from the control group. Hence, we speculate that the potential of C1-C2 pedicle screw techniques for growth limitation was minimal. Furthermore, the rate of malalignment in our study was 26%, and crankshaft phenomenon was not observed at the final follow-up visit, which may be attributed to the short-segment and rigid fixation of C1-C2 pedicle screw techniques. Gluf and Brockmeyer33 reported that the C1-C2 transarticular screw technique did not result in growth deformity in the sagittal or coronal plane. Our study has several limitations. First, the sample size is small because AARD requiring surgery in pediatric patients is rare.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Second, it is a retrospective study. Despite its limitations, we believe that this study successfully assessed long-term outcomes (minimum 5 years) after application of C1-C2 pedicle screw techniques to treat pediatric AARD.
REFERENCES 1. Desai R, Stevenson CB, Crawford AH, Durrani AA, Mangano FT. C-1 lateral mass screw fixation in children with atlantoaxial instability: case series and technical report. J Spinal Disord Tech. 2010;23:474-479. 2. Menezes AH. Craniocervical fusions in children. J Neurosurg Pediatr. 2012;9:573-585. 3. Chen ZD, Wu J, Lu CW, Zeng WR, Huang ZZ, Lin B. C1eC2 pedicle screw fixation for pediatric atlantoaxial dislocation [e-pub ahead of print]. J Pediatr Orthop. 2017. https://doi.org/10.1097/ BPO.0000000000001111. 4. Guo X, Xie N, Lu X, Guo Q, Deng Y, Ni B. Onestep reduction and fixation applying transposterior arch lateral mass screw of C1 combined with pedicle screw of C2 and rod system for pediatric acute atlantoaxial rotatory subluxation with injury of transverse ligament. Spine (Phila Pa 1976). 2015;40:E272-E278. 5. Zhang YH, Shao J, Chou D, Wu JF, Song J, Zhang J. C1-C2 pedicle screw fixation for atlantoaxial dislocation in pediatric patients younger than 5 years: a case series of 15 patients. World Neurosurg. 2017;108:498-505. 6. Fielding JW, Hawkins RJ. Atlanto-axial rotatory fixation. (Fixed rotatory subluxation of the atlanto-axial joint). J Bone Joint Surg Am. 1977;59: 37-44. 7. Tan M, Wang H, Wang Y, Zhang G, Yi P, Li Z, et al. Morphometric evaluation of screw fixation in atlas via posterior arch and lateral mass. Spine (Phila Pa 1976). 2003;28:888-895. 8. Yi P, Dong L, Tan M, Wang W, Tang X, Yang F, et al. Clinical application of a revised screw technique via the C1 posterior arch and lateral mass in the pediatric population. Pediatr Neurosurg. 2013;49:159-165. 9. Buchowski JM, Liu G, Bunmaprasert T, Rose PS, Riew KD. Anterior cervical fusion assessment: surgical exploration versus radiographic evaluation. Spine (Phila Pa 1976). 2008;33:1185-1191. 10. Ma H, Dong L, Liu C, Yi P, Yang F, Tang X, et al. Modified technique of transoral release in onestage anterior release and posterior reduction for irreducible atlantoaxial dislocation. J Orthop Sci. 2016;21:7-12. 11. Rodgers WB, Coran DL, Kharrazi FD, Hall JE, Emans JB. Increasing lordosis of the occipitocervical junction after arthrodesis in young children: the occipitocervical crankshaft phenomenon. J Pediatr Orthop. 1997;17:762-765. 12. Goel A, Shah A. Atlantoaxial facet locking: treatment by facet manipulation and fixation. Experience in 14 cases. J Neurosurg Spine. 2011;14:3-9.
CONCLUSIONS C1-C2 pedicle screw techniques are safe and effective for the treatment of AARD and result in no obvious limitation on growth in older children.
13. Neal KM, Mohamed AS. Atlantoaxial rotatory subluxation in children. J Am Acad Orthop Surg. 2015;23:382-392. 14. Ishii K, Chiba K, Maruiwa H, Nakamura M, Matsumoto M, Toyama Y. Pathognomonic radiological signs for predicting prognosis in patients with chronic atlantoaxial rotatory fixation. J Neurosurg Spine. 2006;5:385-391. 15. Chechik O, Wientroub S, Danino B, Lebel DE, Ovadia D. Successful conservative treatment for neglected rotatory atlantoaxial dislocation. J Pediatr Orthop. 2013;33:389-392. 16. Hicazi A, Acaroglu E, Alanay A, Yazici M, Surat A. Atlantoaxial rotatory fixation-subluxation revisited: a computed tomographic analysis of acute torticollis in pediatric patients. Spine (Phila Pa 1976). 2002;27:2771-2775. 17. Wang S, Yan M, Passias PG, Wang C. Atlantoaxial rotatory fixed dislocation. Spine (Phila Pa 1976). 2016;41:E725-E732. 18. Deichmueller CM, Welkoborsky HJ. Grisel’s syndrome—a rare complication following “small” operations and infections in the ENT region. Eur Arch Otorhinolaryngol. 2010;267:1467-1473. 19. Tauchi R, Imagama S, Ito Z, Ando K, Muramoto A, Matsui H, et al. Surgical treatment for chronic atlantoaxial rotatory fixation in children. J Pediatr Orthop B. 2013;22:404-408. 20. Pang D, Li V. Atlantoaxial rotatory fixation: part 2— new diagnostic paradigm and a new classification based on motion analysis using computed tomographic imaging. Neurosurgery. 2005;57:941-953. 21. Ishii K, Matsumoto M, Momoshima S, Watanabe K, Tsuji T, Takaishi H, et al. Remodeling of C2 facet deformity prevents recurrent subluxation in patients with chronic atlantoaxial rotatory fixation: a novel strategy for treatment of chronic atlantoaxial rotatory fixation. Spine (Phila Pa 1976). 2011;36:E256-E262. 22. Matsumoto Y, Mizutani J, Suzuki N, Otsuka S, Hayakawa K, Fukuoka M, et al. Temporary internal fixation using C1 lateral mass screw and C2 pedicle screw (Goel-Harms technique) without bone grafting for chronic atlantoaxial rotatory fixation. World Neurosurg. 2017;102:696.e1-696.e6. 23. Kato G, Kawaguchi K, Tsukamoto N, Komiyama K, Mizuta K, Onohara T, et al. Recurrent dislocations of the atlantooccipital and atlantoaxial joints in a halo vest fixator are resolved by backrest elevation in an elevation angle-dependent manner. Spine J. 2015;15:e69-e74. 24. Limpaphayom N, Skaggs DL, McComb G, Krieger M, Tolo VT. Complications of halo use in children. Spine (Phila Pa 1976). 2009;34:779-784. 25. Aryan HE, Newman CB, Nottmeier EW, Acosta FL, Wang VY, Ames CP. Stabilization of
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
the atlantoaxial complex via C-1 lateral mass and C-2 pedicle screw fixation in a multicenter clinical experience in 102 patients: modification of the Harms and Goel techniques. J Neurosurg Spine. 2008;8:222-229. 26. Yang F, Dong L, Tan M, Ma H, Yi P, Tang X. In vivo analysis of cervical range of motion after revised C1-C2 pedicle screw technique for pediatric atlantoaxial instability. Pediatr Neurosurg. 2014;49:282-286. 27. Wills BP, Jencikova-Celerin L, Dormans JP. Cervical spine range of motion in children with posterior occipitocervical arthrodesis. J Pediatr Orthop. 2006;26:753-757. 28. Ishikawa M, Matsumoto M, Chiba K, Toyama Y, Kobayashi K. Long-term impact of atlantoaxial arthrodesis on the pediatric cervical spine. J Orthop Sci. 2009;14:274-278. 29. Kanna PR, Shetty AP, Rajasekaran S. Anatomical feasibility of pediatric cervical pedicle screw insertion by computed tomographic morphometric evaluation of 376 pediatric cervical pedicles. Spine (Phila Pa 1976). 2011;36:1297-1304. 30. Anderson RC, Ragel BT, Mocco J, Bohman L-E, Brockmeyer DL. Selection of a rigid internal fixation construct for stabilization at the craniovertebral junction in pediatric patients. J Neurosurg. 2007;107(1 suppl):36-42. 31. Galindo MJ, Francis WR. Atlantal fracture in a child through congenital anterior and posterior arch defects. A case report. Clin Orthop Relat Res. 1983;178:220-222. 32. Ogden JA. Radiology of postnatal skeletal development. XI. The first cervical vertebra. Skeletal Radiol. 1984;12:12-20. 33. Gluf WM, Brockmeyer DL. Atlantoaxial transarticular screw fixation: a review of surgical indications, fusion rate, complications, and lessons learned in 67 pediatric patients. J Neurosurg Spine. 2005;2:164-169. Conflict of interest statement: This work was supported by grants from Capital Characteristic Clinical project of Beijing Municipal Science and Technology Commission (http://www. bjkw.gov.cn/n8785584/index.html) (Grant No. Z161100000516009). No individuals employed or contracted by the funders played any role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Received 20 February 2018; accepted 9 April 2018 Citation: World Neurosurg. (2018) 115:e404-e421. https://doi.org/10.1016/j.wneu.2018.04.062 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
e411
ORIGINAL ARTICLE XINJIE WU ET AL.
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
SUPPLEMENTARY DATA
Supplementary Figure 2. Part of the control group, case 2.
Supplementary Figure 1. Part of the control group, case 1.
e412
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 3. Part of the control group, case 3.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 4. Part of the control group, case 4.
www.WORLDNEUROSURGERY.org
e413
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 5. Part of the control group, case 5.
e414
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 6. Part of the control group, case 6.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 7. Part of the control group, case 7.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 8. Part of the control group, case 8.
www.WORLDNEUROSURGERY.org
e415
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 9. Part of the control group, case 9.
e416
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 10. Part of the control group, case 10.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 11. Part of the control group, case 11.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 12. Part of the control group, case 12.
www.WORLDNEUROSURGERY.org
e417
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 13. Part of the control group, case 13.
e418
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 14. Part of the control group, case 14.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 15. Part of the control group, case 15.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 16. Part of the control group, case 16.
www.WORLDNEUROSURGERY.org
e419
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 17. Part of the control group, case 17.
e420
www.SCIENCEDIRECT.com
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 18. Part of the control group, case 18.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.04.062
ORIGINAL ARTICLE XINJIE WU ET AL.
Supplementary Figure 19. Part of the control group, case 19.
WORLD NEUROSURGERY 115: e404-e421, JULY 2018
C1-C2 PEDICLE SCREW TECHNIQUES FOR PEDIATRIC AARD
Supplementary Figure 20. Part of the control group, case 20.
www.WORLDNEUROSURGERY.org
e421