This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/authorsrights
Author's personal copy
Spine Deformity 2 (2014) 131e142 www.spine-deformity.org
Scoliosis-Associated Cervical Spine Pathologies Mehmet B. Balio glu, MDa,*, Akif Albayrak, MDa, Yunus Atıcı, MDa, Mehmet T. Tacal, MDa, Mehmet A. Kaygusuz, MDa, Can H. Yıldırım, MDb, Miktat Kaya, MDb, Erol Tas‚demiroglu, MDb, Aytac‚ Akbas‚ak, MDb a
Department of Orthopaedics and Traumatology, Disease of the Spine Surgery Group, Metin Sabanci Baltalimani Disease of the Bone Education and Research Hospital, Rumeli Hisari cd No: 62, 34470 Baltalimani Istanbul, Turkey b Department of Neurosurgery, Kafkas University, School of Medicine, Kafkas Universitesi Kampusu Saglik Arastirma ve Uygulama Hastanesi, 36100 Kars, Turkey Received 2 August 2012; revised 16 September 2013; accepted 2 November 2013
Abstract Study Design: A total of 126 scoliosis patients admitted to the hospital were screened for concomitant cervical pathologies. Objectives: To investigate the prevalence of cervical spine pathologies and the clinical relevance of magnetic resonance imaging (MRI) in the evaluation of patients with neuromuscular, congenital, syndromic, and idiopathic scoliosis. Background Summary: With the development of MRI, upper neural axis abnormalities such as syringomyelia and Chiari malformation are increasingly being found in patients with scoliosis, but no report in the literature describes other pathologies in the cervical area seen concomitant with different scoliosis types. Methods: A total of 126 consecutive patients who were classified as having neuromuscular, congenital, syndromic, and idiopathic scoliosis were retrospectively evaluated. Data regarding cervical neural axis abnormalities obtained from the MRI studies were analyzed and classified into each type of scoliosis group. Results: A total of 126 patients with scoliosis were evaluated for hindbrain and cervical spine anomalies. Patients were divided into 4 groups regarding the type of scoliosis. The cervical spine of all patients was evaluated with MRI and other radiologic methods when needed. The most frequently seen pathology was syringomyelia. Other pathologies found included congenital vertebral anomalies, Chiari malformation, arachnoid cyst, atlanto-axial dissociation, split cord, posterior vertebral fusion, vertebral hypoplasia, neurenteric cyst, myelomalacia, dermoid cyst, and decrease in craniovertebral angle. Cervical pathologies were most frequently seen in neuromuscular scoliosis, followed by congenital and syndromic groups. Conclusions: Cervical spinal pathologies vary according to the type of scoliosis. The number of cervical spinal pathologies diagnosed in idiopathic scoliosis patients was least compared with neuromuscular and syndromic groups. The most common pathology was syringomyelia, followed by congenital vertebral anomalies and cerebral tonsillar hernia. Preoperative MRI scan provides vital information regarding cervical spinal pathologies encountered in scoliosis patients. Ó 2014 Scoliosis Research Society. Keywords: Scoliosis; Cervical spinal pathologies; Magnetic resonance imaging; Neural axis abnormalities; Syringomyelia
Introduction Magnetic resonance imaging (MRI) scanning in spinal deformity is often aimed at identifying possible underlying Author disclosures: MBB (none); AA (none); YA (none); MTT (none); MAK (none); CHY (none); MK (none); ET (none); AA (none). *Corresponding author. Department of Orthopaedics and Traumatology, Disease of the Spine Surgery Group, Metin Sabanci Baltalimani Disease of the Bone Education and Research Hospital, Rumeli Hisari cd No: 62, 34470 Baltalimani Istanbul, Turkey. Tel.: þ90 5322521483; fax: þ90 2123230147. E-mail address:
[email protected] (M.B. Balioglu). 2212-134X/$ - see front matter Ó 2014 Scoliosis Research Society. http://dx.doi.org/10.1016/j.jspd.2013.11.001
correctable causes of deformity and conditions that should be treated before surgical correction of the curve itself. Any patient with an unusual, painful, or rapidly progressing curve should undergo an MRI, but routine MRI scanning preoperatively is not indicated in neurologically normal typical adolescent idiopathic scoliosis (AIS) [1]. Intraspinal anomalies were shown in 20% to 38% of patients with congenital, infantile, and juvenile scoliosis [2-6]. The incidence of intraspinal abnormalities reported in patients with congenital spinal deformity ranged from 15% to 43% [7-13]. Although intraspinal anomalies are rarely found in AIS, the risk increases with left thoracic curves, apical
Author's personal copy
132
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
kyphosis, rapidly changing myelodysplastic curves, congenital curves, or any condition with progressive abnormal neurologic findings [14-16]. Furthermore, underlying entities such as Chiari malformations (CM), syringomyelia, cord tethering, or intramedullary spinal cord tumors must be diagnosed because they may present with scoliosis but without neurologic signs. The most common intraspinal anomaly with scoliosis is Chiari malformation type I (CM-I) or only syringomyelia [14]. The other most common anomalies are tethered cord, lipoma, diastematomyelia, or fatty filum. There has been an increase in CM-I and syringomyelia in patients with spinal deformity since the beginning of 1990s, when MRI was first used. It was shown that 50% to 90% of patients with CM were associated with scoliosis and that 15% to 65% of patients with CM-I had scoliosis [17]. It was reported that scoliosis could develop alone without syringomyelia with CM-I [18]. When correction of scoliosis deformity is necessary, pathologies increase the risk of neurological injury by tethering the spinal cord [19,20]. Therefore, if there are intraspinal pathologies, a neurosurgical evaluation and treatment before deformity surgery are necessary because there is a risk of neurological deterioration during the deformity correction [21-24]. The incidence of tethered cord with CM-I was reported to be 14% [25-28]. Thus, it is advisable to correct intraspinal anomalies before decompression of CM [25,26,29,30]. Proposed indications to perform MRI screening include early/juvenile onset, atypical curvature, double thoracic curve, rapid progression, male gender, abnormal neurologic findings, and sagittal profile of the spine and the presence of pain [31,32]. In recent years, studies performed by using MRI have shown an increase in the number of osseous spinal and neural pathologies. It has been reported that neurologic symptoms accompanying osseous spine anomalies manifested themselves at the third and fourth decades of life without being noticed previously [33]. Pathologies accompanying scoliosis in the cervical area include intraspinal and osseous pathologies such as CM, diastematomyelia, syringomyelia, lipoma and lipomeningocele, teratomas, neurenteric cyst, dermoid cyst, epidermoid cyst, dysmorphic atlas, os odontoideum, C2eC3 fusion, basilar invagination, spinal canal stenosis, occipitoatlantal instability, atlanto-axial instability, canal encroachment, myelomalacia, neurofibromatosis [34], cervical and thoracic hemivertebrae, astrocytoma, and brain stem tumor [7,32-38]. The most common cervical pathology encountered in patients with scoliosis is syringomyelia. In patients with idiopathic scoliosis and accompanying syringomyelia, serious neurological complications have been reported after surgical interventions performed to correct scoliosis without decompressing neurologic tissues before the correction operation [39]. Because congenital spine anomalies can be seen in cervical as well as thoracic and lumbar regions, whole spinal axis should be screened, including the cervical region [37]. The associated cervical
anomalies may cause complications during the treatment of scoliosis, especially during the distraction. Exploration of neural axis anomalies and osseous pathologies before surgery for scoliosis is extremely important. There are reports in the literature correlated with MRI findings of whole vertebral axis with scoliosis; and the current study on patients with different types of scoliosis emphasizes the importance of concomitant cervical spinal disorders using MRI. The objectives of this study were to define cervical spine pathologies during MRI investigation of the whole spinal axis in patients with scoliosis, and to classify these pathologies according to the type of scoliosis (ie, infantile and juvenile idiopathic [IS], congenital [CS], neuromuscular [NS], and syndromic [SS]). Materials and Methods In this study, patients with scoliosis admitted to the hospital consecutively between 2000 and 2010 with curves greater than 20 were examined retrospectively for MRI analyses of the craniovertebral junction to sacrococcygeal region, and evaluated their cervical spine regions. Magnetic resonance images of the cervical pathologies were classified according to scoliosis type. T1W1 and STIR weighted sagittal, and T1W1 coronal and axial images of the cervical, thoracic, lumbar, and sacrococcygeal regions of the spine were examined using 1.5-T magnetic resonance equipment. A T1W1 sequence was used to evaluate the morphology of the bony structure, vertebral anomalies, osseous tumors, lipoma of the filum terminale, and CM. A T2W1 sequence was used to differentiate among syrinx, tethered cord, or lipomas; and T2W1 and STIR sequences were employed in the evaluation of tethered cord, syrinx, and tumors. The radiographic features were CM, syringomyelia, congenital vertebral anomalies, atlanto-axial dissociation, split cord (diastematomyelia), vertebral hypoplasia, and a decrease in the craniocervical angle. Inclusion criteria for the study were curve greater than 20 , definite diagnosis of CS, NS, SS, and onset of IS at less than 10 years of age, patients with completely documented data of medical records, plain radiograph, and MRI of the whole spine preoperatively. Exclusion criteria were pure kyphosis and onset of IS at greater than 10 years of age. For the diagnosis of the Chiari malformation has been measured as cerebellar tonsil herniation O4 to 5 mm below the foramen magnum [40]. Principally patients with intraspinal pathologies were planned before deformity correction; therefore, detection of intraspinal anomalies with MRI was evaluated by neurosurgery. Results A total of 126 patients had scoliosis. Patients were separated into 4 cohorts according to scoliosis type. There were 48 patients (38%) with CS, 44 (34.9%) with NS, 20 (15.8%) with SS, and 14 (11.1%) with IS (infantile or juvenile) in each group. Magnetic resonance imaging
Author's personal copy
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
133
Table 1 Types of scoliosis.
Neuromuscular Congenital Syndromic Idiopathic Total/Average
Gender (female/ male)
Mean age, years
Patients per group
Patients with cervical pathologies, n (%)
Pathologies, n (%)
12/5 10/3 0/4 0/0 22/12
15.3 15 14 6 12.5 (1e35)
44 48 20 14 126
17 (38.6%) 13 (27%) 4 (20%) 0 34
25 (44.6%) 17 (30.3%) 4 (7.1%) 0 46
examinations showed cervical pathologies in 22 females (64.7%) and 12 males (35.3%). The mean age was 12.5 years (range, 1e35 years) in these groups. Cervical pathologies were distributed according to the type of scoliosis (Table 1). When the overall patient group was considered, there were 46 different cervical pathologies in 34 patients (26.9%). The most frequent pathology was syringomyelia, with a 34.7% rate (16 patients); other pathologies were congenital vertebral anomalies (26%; 12 patients), CM (19.5%; 9 patients), atlanto-axial dissociation (6.5%; 3 patients), arachnoid cyst (4.3%; 2 patients), split cord (4.3%; 2 patients), vertebral hypoplasia (2.1%; 1 patient), neurenteric cyst (2.1%; 1 patient), myelomalacia (2.1%; 1 patient), dermoid cyst (2.1%; 1 patient), and a decrease in craniovertebral angle (2.1%; 1 patient) (Table 2). Cervical pathologies were seen most frequently in the NS group, followed by the CS and SS groups (Table 3). The mean age of patients with NS (44 patients; 34.9%) was 8.4 (range, 1e30 years). Of these, 30 were female (68.2%) and 14 were male (31.8%). The total number of cervical pathologies was 25 (54.3%), including 7 syringomyelia, 7 cerebellar tonsillar herniations, 4 congenital vertebral anomalies, 2 atlanto-axial dislocations, 2 arachnoid cysts, 1 myelomalacia, 1 diastematomyelia, and 1 decreased craniocervical angle. Furthermore, 17 of these 44 patients with NS (38.6%) were operated on for different intraspinal pathologies (12 females and 5 males; mean age, 15.5 years). Moreover, just 3 of these 17 patients (6.8%) required posterior spinal surgery and fusion on the cervical area; 2 of these 3 patients (4.5%) were CM and 1 (2.2%) was operated Table 2 Frequency of all cervical pathologies. Pathology
Cervical, n (%)
Syringomyelia Congenital vertebral anomaly Chiari malformation Atlanto-axial dissociation Arachnoid cyst Split cord (diastematomyelia) Vertebral hypoplasia Neuroenteric cyst Myelomalacia Dermoid cyst Decrease in cranioservical angle Total
13 12 9 3 2 2 1 1 1 1 1 46
(28.2%) (26%) (19.5%) (6.5%) (4.3%) (4.3%) (2.1%) (2.1%) (2.1%) (2.1%) (2.1%)
on for a neuroectodermal cyst (Fig. 1). The mean age of patients with CS (48 patients; 38%) was 9.8 years (range, 1e32 years); 17 were males (35.4%) and 31 were females (64.6%). The CS group consisted of 13 patients (27%) (10 females and 3 males), with a mean age of 15 years. The distribution of 17 different pathologies (36.9%) was 8 congenital vertebral anomalies, 4 syringomyelia, 2 cerebellar tonsillar herniations, 1 vertebral hypoplasia, 1 split cord, and 1 neurenteric cyst. Furthermore, 5 of these 48 patients (11.3%) underwent surgery by intraspinal pathologies, and 6 of these 48 patients (13.6%) were corrected by posterior instrumentation. No patients with SS needed surgery for cervical pathologies. Twenty patients (15.8%) with SS were evaluated; results included were Escobar (2), Marfan (2), spondylo-epiphysial dysplasia (2), Larsen (2), Ganoderma osteodystrophia (2), Pierre Robin syndrome (1), 9P (1), Desbuquios (1), RubinsteineTaybi (1), DiGeorge (1), Eisenmenger (1), Gilbert (1), Morquio (MPS Tip IV A) (1), hereditary motor and sensory neuropathy Tip 4 (1), and 1P deletion (1). Four patients (20%) had intraspinal pathologies upon MRI. All 4 patients with SS were males with a mean age of 14 years. These 4 cervical pathologies (8.7%) included 2 syringomyelia, 1 atlanto-axial dissociation, and 1 dermoid cyst. All of the patients with SS did not need surgery for cervical pathologies. The mean age of the 14 IS patients under 10 years of age (11.1%) was 3.2 years (range, 1e9 years); 2 of these were male (14.2%) and 12 were female (85.8%). In the IS group, no cervical pathology was found upon MRI. Only 2 patients were operated on because of an increase in the deformity (Table 4). No problems were encountered in MRI during anesthesia. Other organ anomalies and orthopedic problems accompanied NS, CS, and SS. In particular, patients with spina bifida had lower extremity motor and sensorial disfunction, bowel and bladder disturbance, and neurological impairment with pathological reflex. No neurological disturbances were seen in patients with IS under 10 years of age. In this study, 24 of 126 patients (19%) underwent neurosurgical intervention in different areas of the spine. Of these 24 patients, 13 (54%) had myelomeningocele repairs, 8 (33.3%) tethered cord releases, 2 (8.3%) suboccipital decompression and duraplasty, and 1 (4.1%) excision of the cervicothoracic neuroenteric cyst. When these patients were evaluated according to their etiologies, 18 (75%) were NS, 5 (20.8%) were CS, and 1 (4.1%) was SS. However, of
Author's personal copy
134
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
Table 3 Distribution of cervical pathologies in all groups. Neuromuscular Syringomyelia Serebellar tonsillar hernia Conjenital vertebral anomaly Atlanto-axial dissociation Arachnoid cyst Split cord (diastemetamyleia) Neuroenteric cyst Myelomalacia Dermoid cyst Decrease in cranioservical angle Vertebral hypoplasia Total
7 7 4 2 2 1
Congenital 4 2 8
Syndromic
Idiopathic
Total
0
13 9 12 3 2 2 1 1 1 1 1 46
2
1 1 1
1 1 1 25
all 126, just 3 (2.3%) with NS required cervical spinal surgery. In addition, in 13 of these 24 patients, neurosurgical intervention was required after an average of 4.7 years (range, 6 months to 19.8 years), including posterior instrumentation and fusion using pedicle screws (6), rib distraction device or Vertical Expandable Titanium Rib techniques (4), growing rods (1), epiphysiodesis (1), and hemivertebra excision (1). According to etiologies, techniques included posterior instrumentation and growing rod with NS (4); posterior instrumentation, hemivertebra excision, growing rod, Vertical Expandable Titanium Rib, and posterior convex epiphysiodesis with CS (6); and posterior instrumentation with SS (3). Intraspinal pathologies in patients with 1 SS and 1 CS were operated on using posterior instrumentation without an intraspinal approach. One patient with spina bifida, CM, and syringomyelia was
1 17
4
operated on by posterior instrumentation 18 years after the initial operation because of myelomeningocele repair without the need for CM treatment (Fig. 2). No patients developed neurological impairment during or after deformity correction. Discussion Magnetic resonance imaging is a noninvasive technique that provides multiplanar imaging without the use of ionizing radiation. It offers superior soft tissue characterization, facilitates visualization of complex anatomy, and permits accurate assessment of the entire neural axis [41]. In recent years, examinations performed by means of MRI in the spinal axis showed anatomic and pathologic changes, especially in the cervical region. There have been
Fig. 1. Chiari malformation-I neuromuscular scoliosis in an 18-year-old boy CM-I. Suboccipital decompression and duraplasty were applied before 2 years of age owing to due to Chiari malformation-I (A, B). T2e L3 posterior instrumentation and fusion were applied (C, D). Chiari malformation and syringomyelia MRI (E, F).
Author's personal copy
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
135
Table 4 Cervical spine pathologies in neuromuscular, congenital, syndromic and idiopathic scoliosis groups.
Patients, n (%) Patients with cervical pathologies, n (%) Gender (female/male) Age, years (mean [range]) Pathologies, n (%) Syringomyelia Cerebellar tonsillar hernia Congenital vertebral anomalies Atlanto-axial dissociation Arachnoid cyst Myelomalacia Diastometamyelia Decrease in cranioservical angle Neuroenteric cyst Dermoid cyst Vertebral hypoplasia
Neuromuscular
Congenital
Syndromic
Idiopathic
44 (34.9%) 17 (50%) 12/5 15.3 (4e30) 25 (54.3%) 7 7 4 2 2 1 1 1
48 (38%) 13 (38.2%) 10/3 15 (5e35) 17 (36.9%) 4 2 8
20 (15.8%) 4 (11.7%) 0/4 14 (10e18) 4 (8.7%) 2
14 (11.1%) 0 12/2 3.2 (1e9) 0
significant increases in the incidence of CM [32] and syringomyelia [35] in patients with AIS. Although the embryological explanation for variations of the upper cervical spine is unclear, abnormalities likely arise during somatogenesis as a result of errors in cellular proliferation, migration, differentiation, and segmentation [42]. Several reports indicated that primary dysfunction of the brain stem and spinal cord contribute to the pathogenesis of IS. After a study in which scoliosis developed after experimentally induced syringomyelia in dogs, Chuma et al. [43] proposed that dysfunction of the central nervous system may contribute to the pathogenesis of spinal deformities. Chu et al. [44] found significantly lower cerebellar tonsils in patients with AIS compared with normal controls. The diameter of the foramen magnum was considerably longer in patients with AIS than in normal controls, but it has been proven that this anomaly does not cause changes in cerebrospinal fluid flow velocity. The CM is a condition characterized by herniation of the posterior fossa contents below the level of the foramen magnum, and is categorized into 3 types based on the degree of herniation. Type I CM is
1
1 1 1 1
characterized by caudal descent of the cerebellar tonsils and is associated with hydromyelic cavitation of the spinal cord in 50% to 76% of patients [45]. In recent years, since the advent of MRI, an increasing number of asymptomatic, doubtfully symptomatic, and minimally symptomatic patients with CM-I have been diagnosed. This has resulted in controversy about the multiple therapeutic strategies indicated for these problems. It is believed that herniation of the cerebellar tonsils obstructs the cerebrospinal fluid [46,47]. In children, possibly with CS, there may be upper extremity weakness and cranial nerve palsy. Deficiency after closing the neural fold leads to undeveloped basichondrocranium. It is believed that small and shallow posterior fossa results [46,48,49]. Neural abnormalities in the spine are seen associated with diastematomyelia, tethered cord, syrinx, CM, Dandy Walker malformation, intradural lipoma, and arachnoid cyst. In these situations, MRI is available as a diagnostic method to understand them. For instability, dynamic cervical MRI can be performed under observation for spinal cord compression [50]. In a study conducted by Nakahara et al. [31], all spinal
Fig. 2. Chiari malformation-II neuromuscular scoliosis with spina bifida in an 18-year-old girl who was operated on for myelomeningocele at 1 year of age. Deficiencies in the lumbar posterior vertebrae, tethered cord, and Chiari malformation (A, B). Progressive scoliosis (C, D). T2-sacroilac posterior instrumentation and fusion were applied (E, F).
Author's personal copy
136
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
pathologies found in the AIS group, which had 18 patients, were in the cervical region. The incidence of neural axis anomalies with MRI in 472 patients with AIS was 3.8% (18 patients); 6 patients had CM-I, 10 had CM-I with syringomyelia, and 2 had only syringomyelia. With MRI, the researchers found significant neural axis abnormalities in males younger than 11 years of age and with abnormal superficial abdominal reflex. Even through there was no specific indication for early diagnosis of the neural axis abnormalities, preoperative planning was recommended for routine use. Gupta et al. [35] strongly recommend MRI screening in patients with IS of infantile or juvenile onset, especially for those who do not have accompanying neurological symptoms and whose curve angle is more than 20 , because of the high incidence of neural axis anomalies. Especially in the 0- to 10year age group, scoliosis may be the first clue to underlying neural axis anomalies. In a prospective study, those authors examined 34 patients with scoliosis of infantile and juvenile onset; the neural axis anomaly rate was 17.6% (6 of 34 patients). They found CM together with syringomyelia in 1 case and a brain stem tumor in another. On the other hand, in a group with 118 patients, they retrospectively evaluated the rate of neural axis anomalies to be 20.3% (13 of 64) in patients with IS, 16% with CS, and 79% with NS. Gupta et al. found 3 (50%) intraspinal anomalies in 6 infantile idiopathic scoliosis (IIS) patients, 2 of whom needed neurosurgical intervention for CM Inoue et al. [32] suggested that patients with IS whose neurologic status is normal might entail little risk of neurologic complications as a result of scoliosis surgery even if those patients have a neural axis malformation on MRI. Magnetic resonance imaging for the preoperative planning of early-onset scoliosis without clinical symptoms with neural axis anomalies is important [51]. Incidences of neural axis abnormalities in patients with IS were between 2.9% and 37%. Indications for MRI in patients with scoliosis are considered to be early onset, atypical curve, double thoracic curve, fast progression, male gender, and abnormal neurological findings [3,4,14,15,22,23,29,35,40,52-56]. In a prospective trial, Evans et al. [37] performed MRI of the spine and hindbrain in 31 patients with scoliosis with an onset between the ages of 4 and 12 years. In 8 patients (26%), there was a significant neuroanatomical abnormality; there were 6 cases of CM-I associated with a syrinx, 1 isolated CM-I, and 1 astrocytoma of the cervical spine. There were no clinical features that could reliably identify those patients with abnormalities on MRI. In view of the established risks of surgical correction of scoliosis in the presence of undercompressed syringomyelia and the possible improvement that may follow decompression of the foramen magnum, MRI of all patients with scoliosis of juvenile onset should be obligatory [37]. Arnold-CM, syringomyelia, tethered cord, and neoplasm anomalies have been reported in approximately 20% of patients with juvenile IS [35,37,57,58]. In patients with IIS, MRI screening is recommended because of the high prevalence of secondary intraspinal anomalies [3,35,37,57]. Lewonowski et al. [57] found 50% intraspinal anomaly with MRI (2 of 4 patient) in IIS that
had posterior fossa decompression for syrinx with CM-I. Dobbs et al. [3] found a neural axis abnormality upon MRI in 10 of 46 patients (21.7%). That group included 5 patients with an Arnold-CM and an associated cervicothoracic syrinx, 3 with syringomyelia, 1 with low-lying conus, and 1 with brain stem tumor. Because of the high prevalence of abnormalities and the fact that 8 of the 10 patients with abnormal findings on MRI required neurosurgical intervention, a total spine MRI evaluation at the time of presentation is recommended for all patients with IIS who have a curve measuring 20 or more. Pahys et al. [5] reported that MRI revealed a neural axis abnormality in 7 of 54 patients (13%) who underwent an MRI. In that subset of 7 patients, 5 (71.4%) required neurosurgical intervention. Tethered cord requiring surgical release was identified in 3 patients, CM requiring surgical decompression in 2 patients, and a small nonoperative syrinx in 2 patients. This study represents the largest evaluation of intraspinal anomalies in IIS to date. In patients with IIS, MRI screening may be mandatory for fast growing curve (10 /year or more), change in neurological examination, and planning for the correction of the large curve. On the basis of these findings, close observation may be a reasonable alternative to an immediate screening MRI in patients presenting with presumed IIS and a curve greater than 20 . According to Fernandes and Weinstein [59], ‘‘curve progression in the patients with earlyonset scoliosis should be a major indication.’’ Congenital scoliosis is caused by early embryologic errors in vertebral column formation. Defining the deformity, predicting the natural history, and applying the correct treatment can help ensure successful management. Intraspinal abnormalities are present in approximately one third of patients with congenital spine deformities. Curve progression is best documented by measuring identical landmarks on sequential radiographs. Magnetic resonance imaging is warranted when curve progression is established or when surgical intervention is planned [36]. Magnetic resonance imaging of the entire spine and brain stem is mandatory in any child undergoing surgical treatment of a congenital spine deformity. The presence of underlying spinal dysraphism is believed to be upward of 30% in children who have CS [2,6]. Magnetic resonance imaging scans also may be studied to look at the anatomy of the deformity. Magnetic resonance imaging best studies the presence of any cord compression, and this largely has replaced myelography as the imaging modality of choice. The coronal and sagittal images may help define segmentation and formation defects in the anterior spine. The axial views also can be viewed to look at the pedicle anatomy of the patient when contemplating transpedicular instrumentation. Preoperative MRIs can help rule out any coexisting spinal dysraphism. This allows for further imaging of the spinal axis if needed, as well as the ability to clearly image other parts of the thorax and abdomen with MRI in patients who have coexisting organ abnormalities, such as congenital heart disease or urologic abnormalities [60]. Evaluations with MRI before the surgical treatment of congenital spinal deformity have to be made in all children.
Author's personal copy
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
Preoperative MRI may show spinal dysraphism. Spinal dysraphism might be found higher than 30% in patients with CS [25,60,61]. Intraspinal anomalies are associated with hairy patches, sacral dimpling, cavus foot deformity, hyperpigmentation, and/or neurological findings (motor or sensorial deterioration, bladder symptoms, and asymmetrical abdominal reflex). Complete neurological examination is needed even if there are no symptoms of intraspinal anomalies. The nonexistence of these symptoms does not necessarily mean that there are no intraspinal anomalies. Intraspinal anomalies in CS are higher than 38% [6,7,9,10,62,63]. Magnetic resonance imaging shows any existing spinal cord compression; myelography is no longer used. There is risk of the neurological injury during the deformity correction if neural axis abnormalities are not detected [39]. If the spinal cord is fixed with a bone spicule such as diastematomyelia or tethered cord, and is associated with CM and/or syringomyelia or intraspinal tumor, deformity correction may result in spinal cord injury. Curve progression may result from the spinal dysraphism. If the curve shows progression and surgery is planned, MRI is recommended for evaluation of the spinal dysraphism. Using MRI, Prahinski at al. [6] found 9 occult intraspinal anomalies (30%): 5 tethered cord, 4 syringomyelia, 3 lipoma, and 1 diastematomyelia with CS. Two patients (6.6%) needed surgery: 1 with diastematomyelia and 1 with tethered cord. Those authors decided that MRI was beneficial in patients with congenital spinal deformity. According to Belmont et al. [2], 116 patients had CS and a curve that included at least 1 hemivertebra were identified. A total of 76 patients had had MRI and were included in the study. The mean age of those patients at the time of presentation was 4.9 years, and the mean duration of follow-up was 7.7 years. Twenty-nine patients had an isolated hemivertebra and 47 had a complex hemivertebral pattern. Eight of the 29 patients (28%) with an isolated hemivertebra and 10 of the 47 patients (21%) with a complex hemivertebral pattern had an intraspinal anomaly that was detected with MRI. Overall, an abnormal finding on the history or physical examination demonstrated an accuracy of 71%, sensitivity of 56%, specificity of 76%, positive predictive value of 42%, and negative predictive value of 85% for the diagnosis of an intraspinal anomaly. Three patients with an isolated hemivertebra and 5 with a complex hemivertebral pattern underwent neurosurgical intervention. All 8 patients who underwent neurosurgical intervention had had detection of an intraspinal anomaly with MRI, whereas only 4 of those patients (2 of whom had an isolated hemivertebra and 2 of whom had a complex hemivertebral pattern) had had an abnormal finding on either the history or the physical examination. The history and physical examination findings are not predictive of intraspinal anomalies. Therefore, an MRI evaluation of the entire spine should be considered for all patients with CS, including those with an isolated hemivertebra [2].
137
According to Basu [7], intraspinal abnormalities were found in 47 patients (37%). These abnormalities were significantly more common in patients with congenital kyphosis (p 5 .0048) and in those with scoliosis resulting from mixed and segmentation defects. Scoliosis patients with cervical and thoracic hemivertebrae had significantly more intraspinal abnormalities (p 5 .0253) than those with lumbar hemivertebrae. In 64 patients (55%), other organic defects were found. These defects were more common in patients with CS resulting from mixed defects (p 5 .002). Cardiac defects were detected in 26%, and urogenital anomalies in 21% of patients. Magnetic resonance imaging and echocardiography should be an essential part of the evaluation of patients with congenital spinal deformity, and special attention should be paid to patients with segmentation abnormalities, mixed defects, and kyphosis [7]. According to Suh et al. [63], 41 nonrandomized children with congenital spinal deformities (excluding myelomeningocele) who underwent complete MRI evaluation were reviewed. Of the 41 congenital spinal deformities, 37 demonstrated congenital scoliosis, with failure of formation in 19, failure of segmentation in 4, and mixed defects in 14. The remaining 4 deformities were cases of congenital kyphosis. Thirteen patients with congenital spine anomalies had intraspinal abnormalities identified by MRI: tethered cord in 12 patients, syringomyelia in 3, and diastematomyelia in 5. Of the 12 patients with tethered cord, 2 had neurologic deficits. Considering a 31% incidence of intraspinal anomalies, and because clinical manifestations may not be initially detectable, MRI is recommended in patients with congenital spinal deformity as part of the initial evaluation, even in the absence of clinical findings. Congenital cervical scoliosis due to a hemivertebra is an unusual spinal deformity. The congenital cervical scoliosis caused by hemivertebra is a rare but potentially severe spinal deformity. The incidence of hemivertebrae in the cervical spine is low compared with those in the thoracic and lumbar regions. The anomaly is often associated with additional anomalies. The spinal examination also should focus on the cervical spine because of the association of KlippeleFeil syndrome with CS [60]. The most common ones are anomalies in the cervical spine, such as those of congenital block vertebrae (KlippeleFeil syndrome) and CS in the thoracic and lumbar spine [64]. Ozerdemoglu et al. [17] evaluated 105 patients who had both scoliosis and syringomyelia, and subdivided them into 3 groups: 1) 59 patients without CS or myelomeningocele; 2) 20 patients with CS and syringomyelia; and 3) 26 patients with myelomeningocele and syringomyelia. Syringomyelia was diagnosed by surgical exploration (3 patients), myelography (4 patients), myelography followed by delayed computed tomography (9 patients), or MRI (89 patients). Ten of 16 patients in whom the syrinx was not diagnosed by MRI had an MRI at later follow-up. In addition, only 8 of 105 patients were diagnosed before 1980 [17].
Author's personal copy
138
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
With the aid of MRI, syringomyelia with minimal neurologic deficits can be easily diagnosed in patients with scoliosis. Yeom et al. [38] showed that 20 patients with scoliosis with syringomyelia diagnosed by MRI were observed for 6.6 years (range, 2.0e12.6 years) on average. Various factors potentially influencing curve pattern or progression in these patients were then retrospectively reviewed. The location of syrinx was determined using the sagittal view of MRI and the size and the side of syrinx using the T1-weighted axial view of MRI. Eight patients (40%) had small syrinx on MRI according to their classification, 4 (20%) had a medium one, and 8 (40%) had a large one. Syringes with CM-I tended to be larger than those without a malformation. There was no correlation between syrinx size and the size of the major curve of scoliosis. The convex side of the major curve of scoliosis tended to be on the same side as the syrinx and as the unilateral neurologic abnormality. No correlation was found between the location and the size of the syrinx and the location and size of the major curve of the scoliosis, or between the severity of the neurologic deficit and the size of the major curve of the scoliosis. In patients under the age of 10 years at the time of diagnosis of scoliosis and with a flexible curve, decompression of the syrinx improved or stabilized scoliosis. In most patients over the age of 10 years, surgical treatment of the scoliosis was necessary because of the large initial size of the curve or progression of the curve even after syrinx drainage. In the series of Yeom et al. syrinx drainage resulted in neurological improvement and/or in a decrease of syrinx size in all patients, as confirmed by MRI. Therefore, patients with atypical scoliosis such as left thoracic or scoliosis with an unusual appearance, a large curve at a young age, pain or neurologic deficits, less rotation than expected, or headaches of unknown etiology should undergo an MRI to rule out syringomyelia [22,23,38,65,66]. Neurofibromatosis type 1 (NF-1) is a multisystem disease and autosomal dominant genetic disorder. It may manifest as abnormalities of the nervous tissues, bones, soft tissue, and skin. Skeletal abnormalities are common in NF-1. Orthopedic complications usually appear early, including spinal deformities such as scoliosis and kyphosis. The cervical spine should be evaluated at the initial scoliosis assessment. The cervical abnormalities occur more frequently when scoliosis or kyphoscoliosis is present in the thoracolumbar region where the examiner’s attention is focused on the more obvious deformity. The most common cervical abnormality observed is a severe cervical kyphosis, which in itself is highly suggestive of the disorder [34]. The incidence of spinal deformities in association with NF-1 varies from 2% to 36%; scoliosis is the most common. Both heritable and nonheritable factors contribute to the pathogenesis of spinal deformities in NF-1 patients. Traditionally, the spinal deformities are classified as dystrophic or non-dystrophic. The pathophysiology of dystrophic curves is uncertain, but it may require a nonhereditary event such as an adjacent tumor or a second hit event in local bone cells, leading to the underlying dysplasia. Dystrophic curves may result in scoliosis,
kyphosis, or frequently, kyphoscoliosis. The dysplastic features are more commonly associated with deformities of the cervical spine compared with other regions of the spine. Most of the patients with spinal deformities are asymptomatic. When symptoms are present, neck pain is the most common presenting concern. In more severe cases, neurologic deficits may occur, including nerve root compromise and complete or incomplete spinal cord compromise. However, clinical consequences of cervical spine deformities are less marked than in other areas of the spine because the cord versus canal diameter is less critical. If there is suspicion of instability, computed tomography and/or flexion-extension MRI are indicated. The most commonly encountered cervical spine deformity is kyphosis. It may be associated with atlanto-axial instability. Progressive kyphosis is more common than nonprogressive kyphosis. Atlanto-axial instability has been attributed to laxity of capsular and ligamentous structures. Posterior spinal fusion is recommended in patients with cervical spine instability. The level of instability often requires an occipitocervical fusion [67]. The cervical spine is commonly involved in skeletal dysplasias. It is a good general rule to obtain plain cervical spine films on all skeletal dysplasia patients and in those with abnormalities or marked ligamentous laxity, flexionextension views. The most common issues are atlanto-axial instability often associated with odontoid hypoplasia (spondylo-epiphyseal dysplasia, Kneist, mucopolysaccharidosis, pseudoachondroplasia, Stickler syndrome, and metatropic dysplasia), cervical kyphosis (diastrophic dysplasia, camptomelic dysplasia, and Larsen syndrome), and cervical stenosis (achondroplasia, metatropic dysplasia, and Jeune syndrome) [68-74]. Myelopathy from stenosis, kyphosis, or instability can be difficult to detect in infants and young children who have not yet myelinated sufficiently to show spasticity. Sleep studies can be helpful. Flexion-extension MRI can be useful if the radiologist is cooperative, but it is easy to understand why many are reluctant to do flexionextension films on anesthetized patients [74]. The skeletal findings in Loeys-Dietz syndrome (LDS) patient are similar to those found in patients with other connective tissues disorders, including Marfan syndrome. Spinal deformities are most commonly found in the cervical spine. Erkula et al. [75] found cervical spine formation defects or instability in 51% of patients with LDS. Scoliosis was reported in 55% of patients with LDS patients, and dural ectasia was present in 67% [76]. Issues involving the cervical spine occur frequently in children with mucopolysaccharidoses (MPS) and are potentially lives threatening. Spinal cord compression in MPS usually results from a combination of static and dynamic processes: dysplasia of the odontoid process (often an os odontoideum), C1 ring hypoplasia, and C1-C2 ligamentous insufficiency. Glycosaminoglycan accumulation over the odontoid further contributes to stenosis at the occipital-cervical junction. Atlantoaxial instability is extremely common in MPS IV, to the extent that prophylactic fusion has been advocated for children as young as 4 years. At
Author's personal copy
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
present, spinal cord compression in the cervical spine is the most concerning and consistent pathology in these patients. Multilevel cervical stenosis may be present without instability because of dural thickening in the attenuated forms of MPS I (I-HS, I-S, Hurler-Scheie, and Scheie) and in MPS VI [77-81]. Down syndrome is a common genetic disorder that has a significant incidence of spinal pathology. The most common spinal disorder is ligamentous laxity of the cervical spine that involves either the occiput-C1 level, which causes atlanto-occipital instability, or the C1eC2 level, which causes atlanto-axial instability. These areas of cervical instability warrant close monitoring for progressive instability or neurological changes that may require restriction from sports or, in certain cases, surgical stabilization. Down syndrome patients also require close monitoring as they age, because they may also develop acquired degenerative changes in the cervical spine that may result in myelopathy. Scoliosis may also develop in Down syndrome patients; the incidence is unknown. Two primary areas of the cervical spine develop instability. The first is between C1 and C2: atlantoaxial instability, which is primarily caused by laxity of the transverse ligament of C1 and the joint capsules. The second area of instability occurs at the occipitocervical junction and is commonly described as atlanto-occipital instability, which is defined by a Powers ratio of greater than 1 (anterior instability) and less than 0.55 (posterior instability), a basion-axial interval of greater than 12 mm and anteroposterior translational motion described by Weisel et al. to be more than 2 mm. Therefore, certain authors have recommended a flexion-extension MRI scan to evaluate occipitocervical instability and the presence of spinal cord impingement. The third cervical pathological problem that occurs with Down syndrome patients does not result from instability, but from premature and advanced subaxial degenerative changes in the third and fourth decades of life that often result in cervical canal narrowing and resultant myelopathy. Therefore, adult Down syndrome patients who develop decreased or altered ambulatory potential should be screened with MRI to rule out cervical spinal cord compression [82]. Several abnormalities have been noted in Marfan lumbar spine, including pedicular attenuation and widened interpediculate distances. This may result from abnormalities of growth or the presence of dural ectasia. Lumbar pedicle width and laminar thickness are significantly reduced in Marfan individuals. Those with dural ectasia demonstrate increased bony erosion of anterior and posterior elements of lumbosacral spine [83]. Widening of the lumbosacral spinal canal was found in 63% of 57 patients with Marfan syndrome and in none of 57 age- and sex-matched nonMarfan control patients who underwent CT scanning for routine clinical indications. Bony abnormalities in mild cases consisted of thinning of the pedicles and laminae and erosion of the neural foramina and were generally limited to L5 and S1. More severe changes were present in 13 patients, 2 of whom had associated neurologic signs,
139
including meningoceles or near total erosion of a pedicle. Presence and severity of vertebral abnormalities were associated with no other clinical feature or overall phenotypic severity. Dural ectasia can be added to the list of pleiotropic manifestations of Marfan syndrome [84]. Exotic congenital syndromes include conditions that present with unique challenges for spinal deformity treatment. Patients with Jeune syndrome have a high rate of proximal cervical stenosis and should undergo screening with cervical spine films at birth. The deformity may be scoliosis, congenital or early onset, or subtle spine abnormalities, such as C1 stenosis in Jeune syndrome. Arthrogryposis may be associated with a severe scoliosis and jaw contracture may make intubation difficult. Larsen syndrome may have early-onset scoliosis that is rigid and requires early intervention. Cervical kyphosis and subluxation may be lethal in these patients and screening radiographs are important. Upper airway abnormalities are an anesthesia concern. JarchoLevin syndrome is a thoracic volume depletion deformity resulting from shortness of the thorax, either a spondylocostal dysostosis variant or spondylothoracic dysplasia. Klippel-Feil deformity is common, so a cervical spine series with flexion-extension laterals should be obtained to assess for stenosis or instability. Screening MRI of the spinal cord should be obtained to rule out abnormalities, especially in spondylocostal dysostosis. Magnetic resonance imaging studies of the entire spine are mandatory for syndromes that have known a central axis nervous system abnormality, and it is realistic to consider preoperative MRI scan screening of the spinal cord for all patients with exotic congenital syndromes. Occult spinal cord abnormalities that may increase the risk of neurologic injury during operative distraction treatment of the spine in syndromes are often not well characterized in the literature, and MRI scans may detect distal spinal cord tethers, syringomyelia, intradural mass lesions, lateral tethers of the proximal spinal cord, dural ectasia, Arnold-CM, and complex bonee cartilage malformations of the spine that may not be evident on plain radiographs [73]. The risks of neurologic complications during and after the correction of scoliosis are widely known. Syringomyelia may be a risk factor for neurologic complication during the correction of scoliosis, especially during distraction [39]. Ozerdemoglu et al. [17] reported that 3 patients (8%) had a significant deficit after surgery for scoliosis without accomplishing a surgery for syringomyelia before the correction operation. These studies indicate the importance of investigating neural axis abnormalities before corrective surgery for scoliosis; however, there is no prospective study revealing the risk of neurologic complications resulting from scoliosis surgery in patients with asymptomatic neural axis malformations. On the other hand, the routine use of MRI is controversial, and indications for MRI in scoliosis patients vary among authors. Some studies recommend treatment of all syringomyelia before scoliosis correction [17,60,64], whereas others state that routine preoperative MRI is not
Author's personal copy
140
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
necessary in scoliosis patients unless the patient has a neurologic deficit or pain [1,54,85,86]. In the literature, neurosurgical operations for neural abnormalities in patients with IS before scoliosis surgery were 4.5% to 10%. Results of the present large, multicenter study demonstrated a 21.7% prevalence of neural axis abnormalities in otherwise asymptomatic patients with IIS. The high percentage of neural axis abnormalities in these patients is noteworthy because 8 of 10 patients who had such abnormalities required neurosurgical intervention, compared with 50% of juvenile patients with neural axis abnormalities, as reported in the literature [35,57]. Similarly, in the study by Gupta et al. [35], 2 of 3 infantile patients with neural axis abnormalities required neurosurgical intervention. Two of those patients had CM-I associated with a cervicothoracic syrinx, and the third patient had diffuse dural ectasia. All 3 patients were being treated with a brace for correction of the curve at the time of the study. In the study by Lewonowski et al. [57], both patients with neural axis abnormalities required neurosurgical intervention to treat CM-I and an associated syrinx. The report by Dobbs et al. [3] was believed to be the largest multicenter study of patients with IIS to date; there was no association between abnormal findings on MRI and gender, curve magnitude, curve location, or curve direction. However, because of the 21.7% prevalence of abnormal findings on MRI and the fact that 8 of 10 patients with abnormal findings required neurosurgical intervention, they recommended that MRI of the neural axis be performed at the time of presentation for all patients with infantile scoliosis who have a curve measuring 20 , even if the findings of a neuro€ urk et al. [87] logical examination are normal [3]. Ozt€ demonstrated that an 8% prevalence of neural axis abnormalities (20) in 249 patients with adolescent IS; of these only 3 required a neurosurgical intervention, yet none were in the cervical region [87]. Twenty patients with scoliosis with syringomyelia who were diagnosed by MRI were observed for 6.6 years (range, 2.0e12.6 years) on average. In patients under the age of 10 years at diagnosis of scoliosis and with a flexible curve, decompression of the syrinx improved or stabilized scoliosis. In most patients over the age of 10 years, surgical treatment of the scoliosis was necessary because of the large initial size of the curve or progression of the curve even after syrinx drainage. The results of the study of Yeom et al. [38] suggest that early diagnosis and decompression of a syrinx in scoliosis patients especially under the age of 10 years is crucial and may decrease the curve size and limit scoliosis curve progression. The current study retrospectively evaluated cervical spine in patients with IS under 10 years of age and found no neurological abnormalities by MRI. However, there were intraspinal abnormalities in NS (54.3%), CS (35.4%), and SS (20%) patients. Except for 3 patients with NS, neurosurgical intervention was not required in the cervical region. One issue regarding the MRI study is concern about the use of general anesthesia in children when necessary. Despite concerns about sedation, the authors consider MRI
to be essential in the detection of occult spinal anomalies. Some authors believe that neurologically asymptomatic patients with hindbrain and spinal cord abnormalities have little risk of neurologic complications from scoliosis surgery, even when neural axis malformations are shown on MRI [3,32]. Malviya et al. [88] prospectively evaluated 1,140 children (aged 2.96 3.7 years) who were sedated. The medical records of children who experienced adverse events were reviewed. Most children (99%) were monitored with pulse oximetry. Of those children, 239 (20.1%) experienced adverse events related to sedation, including inadequate sedation in 150 (13.2%) and decrease in oxygen saturation in 63 (5.5%). Five children experienced airway obstruction and 2 became apneic. No adverse event resulted in long-term sequelae. According to another study by the same authors, quality assurance data were collected prospectively for children who were sedated (922) or given general anesthesia (140) for MRI or computed tomography. Reasons for pre-selection of general anesthesia included previously failed sedation (28%), potential for failed sedation (32%), and perceived medical risk (14%). Hypoxemia occurred in 2.9% of sedated children, and was more common in children classified as ASA III or IV. Sedation was inadequate for 16% of children and failed in 7% [89]. Especially in terms of anomalies associated with NS, CS, and SS, evaluation with MRI may be important. In the current study on the anomalies associated with scoliosis, surgical treatment was especially necessary in NS. Therefore, the authors believe that the surgeon should know and be informed about these abnormalities before correction surgery. Even if a spinal anomaly is asymptomatic and the patient is neurologically intact, the behavior of these lesions after a curve-correction operation is usually unpredictable. The authors recommend that MRI be performed in all candidates for scoliosis treatment (except for IS) and an agreement be reached by consensus in a multidisciplinary setting in which there is a disparity regarding whether an operation is necessary before the scoliosis correction. Cervical pathologies may differ according to the type of scoliosis. With the MRI study in patients with NS, the cervical pathology rate was as high as 54.4% compared with the other groups, such as 36.9% in patients with CS, 8.7% with SS, and none with infantile or juvenile IS. The most common pathology is syringomyelia, followed by congenital vertebral anomalies and CM, arachnoid cyst, atlantoaxial dissociation, split cord, vertebral hypoplasia, neurenteric cyst, myelomalacia, and dermoid cyst. In the current study, only 3 patients required interventions for the cervical region. These pathologies occurred to a lesser extent in patients with congenital and syndrome-related pathologies. No patients required intervention in the cervical region. No pathologies were seen in the cervical region of IS patients under 10 years of age. The incidence of intraspinal anomalies in the cervical region varies according to the scoliosis etiology. The cervical region in patients with NS, CS, and SS must be evaluated with MRI. Evaluation of the cervical region with MRI for IS patients
Author's personal copy
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
under 10 years of age who have no neurological signs and risk factors may not be necessary; however, a study examining a larger patient population is needed to better define this. Detailed information about cervical pathologies accompanied by scoliosis can be obtained by means of MRI studies. Magnetic resonance imaging evaluation is extremely important for pathologies that cannot be diagnosed by conventional methods. A correct diagnosis would prevent many potential complications from occurring during treatment originating from neural axis malformations.
References [1] Winter RB, Lonstein JE, Heithoff KB, Kirkham JA. Magnetic resonance imaging evaluation of the adolescent patient with idiopathic scoliosis before spinal instrumentation and fusion: a prospective, double-blinded study of 140 patients. Spine (Phila Pa 1976) 1997;22:855e8. [2] Belmont PJ, Kuklo TR, Taylor KF, et al. Intraspinal anomalies associated with isolated congenital hemivertebra: the role of routine magnetic resonance imaging. J Bone Joint Surg Am 2004;86:1704e10. [3] Dobbs MB, Lenke LG, Szymanski DA, et al. Prevalence of neural axis abnormalities in patients with infantile idiopathic scoliosis. J Bone Joint Surg Am 2002;84:2230e4. [4] Hamzaoglu A, Ozturk C, Tezer M, et al. Simultaneous surgical treatment in congenital scoliosis and/or kyphosis associated with intraspinal abnormalities. Spine (Phila Pa 1976) 2007;32:2880e4. [5] Pahys JM, Samdani AF, Betz RR. Intraspinal anomalies in infantile idiopathic scoliosis: prevalence and role of magnetic resonance imaging. Spine (Phila Pa 1976) 2009;34:E434e8. [6] Prahinski JR, Polly DWJ, McHale KA, et al. Occult intraspinal anomalies in congenital scoliosis. J Pediatr Orthop 2000;20:59e63. [7] Basu PS, Elsebaie H, Noordeen MH. Congenital spinal deformity: a comprehensive assessment at presentation. Spine (Phila Pa 1976) 2002;27:2255e9. [8] Bernard Jr TN, Burke SW, Johnston III CE, et al. Congenital spine deformities: a review of 47 cases. Orthopaedics 1985;8:777e83. [9] Bradford DS, Heithoff KB, Cohen M. Intraspinal abnormalities and congenital spine deformities: a radiographic and MRI study. J Pediatr Orthop 1991;11:36e41. [10] McMaster MJ. Occult intraspinal anomalies and congenital scoliosis. J Bone Joint Surg Am 1984;66:588e601. [11] Bollini G, Launay F, Docquier PL, et al. Congenital abnormalities associated with hemivertebrae in relation to hemivertebrae location. J Pediatr Orthop B 2010;19:90e4. [12] Rajasekaran S, Kamath V, Kiran R, et al. Intraspinal anomalies in scoliosis: an MRI analysis of 177 consecutive scoliosis patients. Indian J Orthop 2010;44:57e63. [13] Shen J, Wang Z, Liu J, Xue X, Qiu G. Abnormalities associated with congenital scoliosis: a retrospective study of 226 Chinese surgical cases. Spine (Phila Pa 1976) 2013;38:814e8. [14] Davids JR, Chamberlin E, Blackhurst DW. Indications for magnetic resonance imaging in presumed adolescent idiopathic scoliosis. J Bone Joint Surg Am 2004;86:2187e95. [15] Eule JM, Erickson MA, O’Brien MF, Handler M. Chiari I malformation associated with syringomyelia and scoliosis: a twenty-year review of surgical and nonsurgical treatment in a pediatric population. Spine (Phila Pa 1976) 2002;27:1451e5. [16] Wu L, Qiu Y, Wang B, et al. The left thoracic curve pattern; a strong predictor for neural axis abnormalities in patients with ‘‘idiopathic’’ scoliosis. Spine (Phila Pa 1976) 2010;35:182e5. [17] Ozerdemoglu RA,Transfeldt EE, Denis F. Value of treating primary causes of syrinx in scoliosis associated with syringomyelia. Spine (Phila Pa 1976) 2003;28:806e14.
141
[18] Tubbs RS, Doyle S, Conclin M, Oakes WJ. Scoliosis in a child with Chiari I malformation and the absence of syringomyelia: case report and a review of the literature. Childs Nerv Syst 2006;22:1351e4. [19] Acaroglu E, Alanay A, Akalan N, et al. Risk factors associated with corrective surgery in congenital scoliosis with tethered cord. Turk J Pediatr 1997;39:373e8. [20] McLone DG, Herman JM, Gabrieli AP, Dias L. Tethered cord as a cause of scoliosis in children with a myelomeningocel. Pediatr Neurosurg 1990;16:8e13. [21] Akhtar OH, Rowe DE. Syringomyelia associated scoliosis with and without the Chiari I malformation. J Am Acad Orthop Surg 2008;16: 407e17. [22] Charry O, Koop S, Winter R, et al. Syringomyelia and scoliosis: a review of twenty-five pediatric patients. J Pediatr Orthop 1994;14:309e17. [23] Farley FA, Song KM, Birch JG, Browne R. Syringomyelia and scoliosis in children. J Pediatr Orthop 1995;15:187e92. [24] Potenza V, Weinstein SL, Neyt JG. Dysfunctionof the spinal cord during spinal arthrodesis for scoliosis: recommendations for early detection and treatment. A case report. J Bone Joint Surg Am 1998;80:1679e83. [25] Ayvaz M, Alanay A, Yazıcı M, et al. Safety and efficacy of posterior instrumentation for patients with congenital scoliosis and spinal dysraphism. J Pediatr Orthop 2007;27:380e6. [26] Mehta VA, Gottfried ON, McGirt MJ, et al. Safety and efficacy of concurrent pediatric spinal cord untethering and deformity correction. J Spinal Disord Tech 2011;24:401e5. [27] Reigel DH, Tchernoukha K, Bazmi B, et al. Change in spinal curvature following release of tethered spinal cord associated with spina bifida. Pediatr Neurosurg 1994;20:30e42. [28] Royo-Salvador MB, Sole-Llenas J, Domenech JM, GonzalezAdrio R. Results of the section of the filum terminale in 20 patients with syringomyelia, scoliosis and Chiari malformation. Acta Neurochir 2005;147:515e23. [29] Bhangoo R, Sgouros S. Scoliosis in children with Chiari I-related syringomyelia. Childs Nerv Syst 2006;22:1154e7. [30] Ozerdemoglu RA, Denis F, Transfeldt EE. Scoliosis associated with syringomyelia: clinical and radiologic correlation. Spine (Phila Pa 1976) 2003;28:1410e7. [31] Nakahara D, Yonezawa I, Kobanawa K, et al. Magnetic resonance imaging evaluation of patients with idiopathic scoliosis: a prospective study of four hundred seventy-two outpatients. Spine (Phila Pa 1976) 2011;36:E482e5. [32] Inoue M, Minami S, Nakata Y, et al. Preoperative MRI analysis of patients with idiopathic scoliosis: a prospective study. Spine (Phila Pa 1976) 2004;30:108e14. [33] Hosalkar HS, Sankar WN, Wills BPD, et al. Congenital osseous anomalies of the upper cervical spine. J Bone Joint Surg Am 2008;90: 337e48. [34] Crawford AH, Herrera-Soto J. Scoliosis associated with neurofibromatosis. Orthop Clin N Am 2007;38:553e62. [35] Gupta P, Lenke LG, Bridwell KH. Incidence of neural axis abnormalities in infantile and juvenile patients with spinal deformity: is a magnetic resonance image screening necessary? Spine (Phila Pa 1976) 1998;23:206e10. [36] Hedequist D, Emans J. Congenital scoliosis. J Am Acad Orthop Surg 2004;12:266e75. [37] Evans SC, Edgar MA, Hall-Crags MA, et al. MRI of ‘‘idiopathic’’ juvenile scoliosis: a prospective study. J Bone Joint Surg Br 1996;78:314e7. [38] Yeom JS, Lee C, Park K, et al. Scoliosis associated with syringomyelia: analysis of MRI and curve progression. Eur Spine J 2007;16: 1629e35. [39] Noordeen MH, Taylor BA, Edgar MA. Syringomyelia: a potential risk factor in scoliosis surgery. Spine (Phila Pa 1976) 1994;19:1406e9. [40] Cardoso M, Keating RF. Neurosurgical management of spinal dysraphism and neurogenic scoliosis. Spine (Phila Pa 1976) 2009;34: 1775e82.
Author's personal copy
142
M.B. Balio glu et al. / Spine Deformity 2 (2014) 131e142
[41] Gundry CR, Heithoff KB. Imaging evaluation of patients with spinal deformity. Orthop Clin North Am 1994;25:247e64. [42] Ganey TM, Ogden JA. Development and maturation of the axial skeleton. In: Weinstein SL, editor. The pediatric spine: principals and practice. Philadelphia, PA: Lippincott Williams and Wilkins; 2001. p. 3e54. [43] Chuma A, Kitahara H, Minami S, et al. Structural scoliosis model in dogs with experimentally induced syringomyelia. Spine (Phila Pa 1976) 1997;22:589e94. [44] Chu WCW, Man GCW, Lam WWM, et al. A detailed morphologic and functional magnetic resonance imaging study of the craniocervical junction in adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2007;32:1667e74. [45] Dyste GN, Menezes AH, VanGilder JC. Symptomatic Chiari malformations: an analysis of presentation, management, and longterm outcome. J Neurosurg 1989;71:159e68. [46] Schijman E. History, anatomic forms, and pathogenesis of Chiari I malformations. Childs Nerv Syst 2004;20:323e8. [47] Menezes AH. Primary craniovertebral anomalies and the hindbrain herniation syndrome (Chiari I): data base analysis. Pediatr Neurosurg 1995;23:260e9. [48] Nishikawa M, Sakamoto H, Hakuba A, et al. Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 1997;86:40e7. [49] Hensinger RN. Congenital scoliosis: etiology and associations. Spine (Phila Pa 1976) 2009;34:1745e50. [50] Chan G, Dormans JP. Update on congenital spinal deformities: preoperative evaluation. Spine (Phila Pa 1976) 2009;34:1766e74. [51] Johnston CE. Preoperative medical and surgical planning for early onset scoliosis. Spine (Phila Pa 1976) 2010;35:2239e44. [52] Brockmeyer D, Gollogly S, Smith JT. Scoliosis associated with Chiari I malformations: the effect of suboccipital decompression on scoliosis curve progression: a preliminary study. Spine (Phila Pa 1976) 2003;28:2505e9. [53] Bowman RM, Mohan A, Ito J, et al. Tethered cord release: a longterm study of 114 patients. J Neurosurg Pediatr 2009;3:181e7. [54] Do T, Fras C, Burke S, et al. Clinical value of routine preoperative magnetic resonance imaging in adolescent idiopathic scoliosis: a prospective study of three hundred and twenty-seven patients. J Bone Joint Surg Am 2001;83:577e9. [55] Flynn JM, Sodha S, Lou JE, et al. Predictors of progression of scoliosis after decompression of an Arnold Chiari I malformation. Spine (Phila Pa 1976) 2004;29:286e92. [56] Hankinson TC, Klimo Jr P, Feldstein NA, et al. Chiari malformations, syringohydromyelia and scoliosis. Neurosurg Clin N Am 2007;18:549e68. [57] Lewonowski K, King J, Nelson M. Routine use of magnetic resonance imaging in idiopathic scoliosis patients less than eleven years of age. Spine (Phila Pa 1976) 1992;17(Suppl):109e16. [58] Benli IT, Uzumcugil O, Aydin E, et al. Magnetic resonance imaging abnormalities of neural axis in Lenke type 1 idiopathic scoliosis. Spine (Phila Pa 1976) 2006;31:1828e33. [59] Fernandes P, Weinstein SL. Natural history of early onset scoliosis. J Bone Joint Surg Am 2007;89(Suppl 1):21e33. [60] Hedequist DJ. Surgical treatment of congenital scoliosis. Orthop Clin N Am 2007;38:497e509. [61] Barley JS, Mooney JF, Glazier SS, et al. Sudden appearance of new upper extremity motor function while performing neurophysiologic intraoperative monitoring during tethered cord release: a case report. J Pediatr Orthop 2010;30:624e8. [62] Gillespie R, Faithfull DK, Roth A, et al. Intraspinal anomalies in congenital scoliosis. Clin Orthop Relat Res 1973;93:103e9. [63] Suh S, Sarwark JF, Vora A, Huang BK. Evaluating congenital spine deformities for intraspinal anomalies with magnetic resonance imaging. J Pediatr Orthop 2001;21:525e31. [64] Ruf M, Jensen R, Harms J. Hemivertebra resection in the cervical spine. Spine (Phila Pa 1976) 2005;30:380e5.
[65] Phillips WA, Hensinger RN, Kling TF. Management of scoliosis due to syringomyelia in childhood and adolescence. J Pediatr Orthop 1990;10:351e4. [66] Tomlinson RJ, Wolfe MW, Nadall JM, et al. Syringomyelia and developmental scoliosis. J Pediatr Orthop 1994;14:580e5. [67] Crawford AH, Lykissas MG, Schorry EK, et al. Neurofibromatosis: etiology, commonly encountered spinal deformities, common complications and pitfalls of surgical treatment. Spine Deformity 2012; (Preview Issue):85e94. [68] Letts M, Kabir A, Davidson D. The spinal manifestations of Stickler’s syndrome. Spine (Phila Pa 1976) 1999;24:1260e4. [69] Remes V, Marttinen E, Poussa M, et al. Cervical kyphosis in diastrophic dysplasia. Spine (Phila Pa 1976) 1999;24:1990e5. [70] Coscia MF, Bassett GS, Bowen JR, et al. Spinal abnormalities in camptomelic dysplasia. J Pediatr Orthop 1989;9:6e14. [71] Johnston CE, Birch JG, Daniels JL. Cervical kyphosis in patients who have Larsen syndrome. J Bone Joint Surg Am 1996;78:538e45. [72] Leet AI, Sampath JS, Scott Jr CI, MacKenzie WG. Cervical spinal stenosis in metatropic dysplasia. J Pediatr Orthop 2006;26:347e52. [73] Campbell RM. Spine deformities in rare congenital syndromes: clinical issues. Spine (Phila Pa 1976) 2009;34:1815e27. [74] Sanders JO. Spinal deformity in skeletal dysplasias. Spine Deformity 2012; (Preview Issue): 101e6. [75] Erkula G, Sponseller PD, Paulsen L, et al. Musculoskeletal findings of Loeys-Dietz Syndrome. J Bone Joint Surg Am 2010;92:1876e83. [76] Tan EW, Sponseller PD. Connective tissue syndromes: themes and guidelines for the spine deformity surgeon. Spine Deformity 2012; (Preview Issue): 95e100. [77] Lipson SJ. Dysplasia of the odontoid process in Morquio’s syndrome causing quadriparesis. J Bone Joint Surg Am 1977;59:340e4. [78] Mut M, Cila A, Varli K, et al. Multilevel myelopathy in MaroteauxLamy syndrome and review of the literature. Clin Neurol Neurosurg 2005;107:230e5. [79] Ransford AO, Crockard HA, Stevens JM, et al. Occipito-atlantoaxial fusion in Morquio-Brailsford syndrome: a ten-year experience. J Bone Joint Surg Br 1996;78:307e13. [80] White KK, Steinman S, Mubarak SJ. Cervical stenosis and spastic quadriparesis in morquio disease (MPS IV): a case report with twenty-six-year follow-up. J Bone Joint Surg Am 2009;91:438e42. [81] White KK. Mucopolysaccharidoses: etiology, classification, deformities unique to each type, treatment modalities and indications for surgical intervention. Spine Deformity 2012; (Preview Issue): 114e8. [82] Dimar JY, Carreon LY. Spinal deformity in Down syndrome. Spine Deformity 2012; (Preview Issue): 75e84. [83] Sponseller PD, Ahn NU, Ahn UM, et al. Osseous anatomy of the lumbosacral spine in Marfan syndrome. Spine (Phila Pa 1976) 2000;25:2797e802. [84] Pyeritz RE, Fishman EK, Bernhardt BA, Siegelman SS. Dural ectasia is a common feature of Marfan’s syndrome. Am J Hum Genet 1988;43:726e32. [85] Maiocco B, Deeney VF, Coulon R, Parks PF. Adolescent idiopathic scoliosis and the presence of spinal cord abnormalities: preoperative magnetic resonance imaging analysis. Spine (Phila Pa 1976) 1997;22:2537e41. [86] O’Brien MF, Lenke LG, Bridwell HK, et al. Pre-operative spinal canal investigation in adolescent idiopathic curves greater than 70 degrees. Spine (Phila Pa 1976) 1994;19:1606e10. [87] Ozturk C, Karadereler S, Ornek I, et al. The role of routine magnetic resonance imaging in the preoperative evaluation of adolescent idiopathic scoliosis. Int Orthop 2010;34:543e6. [88] Malviya S, Voepel-Lewis T, Tait AR. Adverse events and risk factors associated with the sedation of children by nonanesthesiologists. Anesth Analg 1997;85:1207e13. [89] Malviya S, Voepel-Lewis T, Eldevik OP, et al. Sedation and general anaes-thesia in children undergoing MRI and CT: adverse events and outcomes. Br J Anaesth 2000;84:743e8.
