Neuromuscular Scoliosis

Introduction

Neuromuscular scoliosis is a type of scoliosis that results from neuromuscular conditions ranging from cerebral palsy (20%-70%) to skeletally immature children with cervical or thoracic level spinal cord injury (100%).^1,2 It is characterized by the following:

• Kyphosis and pelvic obliquity
• Rapid progression at a young age due to early onset of neuromuscular conditions
• Rigid curves from the early onset and limited mobility of the patient
• Risk of progression independent of growth due to neuromuscular imbalance
• Tendency to involve the thoracolumbar spine, creating a long C-shaped curve.

Anatomy

Scoliosis is a three-dimensional deformity involving the coronal plane, sagittal plane, and axial plane of the spinal column. The curve location is based on the apex of curve:

• Cervical: C2-C6
• Cervicothoracic: C7-T1
• Thoracic: T2-T11
• Thoracolumbar: T12-L1
• Lumbar: L2-L4

Lonstein et al further classified the curve pattern of patients with cerebral palsy and mental retardation into two groups by the presence (G-II) or absence (G-I) of pelvic obliquity.⁸

Pathogenesis

The etiology of neuromuscular scoliosis is not completely understood, but likely results from asymmetric muscle strength and tone.

Classification

The classification of neuromuscular scoliosis is based on the underlying disorder responsible for the curve. The Scoliosis Research Society has subdivided neuromuscular scoliosis into neuropathic and myopathic categories.

Neuropathic

Upper motor neuron

• Cerebral palsy
• Spinocerebral degeneration
  • Friedreich’s ataxia
  • Charcot-Marie-Tooth disease
  • Roussy-Levy disease
• Syringomyelia
• Spinal cord tumor
• Spinal cord trauma

Lower Motor Neuron

• Poliomyelitis
• Other viral myelitides
• Trauma
• Spinal muscular atrophy
• Dysautonomic disorders

Myopathic

• Arthrogyroposis
• Muscular dystrophy
• Fiber-type disproportion
• Congenital hypotonia
• Myotonic dystrophy

Natural History

The natural history of neuromuscular spinal deformity is based on curve progression, not etiology. Most neuromuscular scoliosis curves progress from 7º to 40º.^9,10,11 Factors causing curve progression include:

• Early age of onset of neuromuscular disease
• Severe weakness
• Evolving neuromuscular disease
• Skeletal immaturity
• Lack of mobility
• Large curves

The greatest progression usually occurs during the patient’s peak growth, but is also affected by the loss of auto-regulatory spinal alignment from the underlying neuromuscular disorder.

Oda et al have classified Duchenne’s muscular dystrophy into three types of curve progression:¹²

• Type I curves: Characterized by progressive kyphoscoliosis with rotatory deformity extending into the pelvis and reaching 30° before the age of 15 years, with a rapid progression of 15°--20° per year thereafter.
• Type II curves: Characterized by hyperlordosis with a progressive scoliotic deformity. Patients with double major curves have no pelvic obliquity and have stable curves, while patients with lumbar or thoracolumbar curves tend to have pelvic obliquity and progress as Type I curves.
• Type III curves: Have straight sagittal spines and non-progressive scoliotic curves that rarely reach 30°.

Patients with Becker’s muscular dystrophy tend to have mild non-progressive curves because they are older and skeletally mature.¹³ However, patients with cerebral palsy tend to have curves that progress into adulthood.^11,14

Clinical Presentation

A thorough history (perinatal, developmental, and family) and physical are essential when diagnosing neuromuscular scoliosis. Clues that suggest neuromuscular scoliosis include birth anoxia, delayed developmental milestones, acquired or familial neuropathies/myopathies, spinal deformity before the age of 7 years, or a painful scoliosis.

When performing the physical, the following should be evaluated:

• Height and weight
• Head tilt
• Shoulder elevation
• Pelvic obliquity
  • Suprapelvic is a continuation of curve
  • Infrapelvic results from hip contracture
  • Intrapelvic is secondary to morphologic changes of the hemi-pelvises
• Overall trunk balance
• Rib cage deformities
• Skin for signs of stigmata that may represent an underlying pathologic condition
  • Café au lait spots and axillary freckles associated with neurofibromatosis
  • Hairy patches and midline nevi associated with intradural pathologies
• Neurologic status
  • Strength
  • Sensation
  • Reflexes (particularly abdominal)
• Inspiratory and expiratory capacity of the chest wall

Imaging and Diagnostic Studies

Radiographic evaluation includes anteroposterior and lateral views of the thoracolumbar spine. If possible, they should be taken in an upright (sitting or standing) position. The coronal Cobb angle is measured. Bending films, traction films, or even intraoperative films with the patient under general anesthesia (with severe spasticity) are helpful in determining curve rigidity.

Patients with neurological signs or symptoms, with neuroectodermal skin lesions, and/or malignant curve progression must have an MRI of the entire spine to assess for any intradural lesions, such as syringomyelia, tethered cord, and spinal tumor.

Pulmonary function tests are important, as patients with neuromuscular scoliosis often have restrictive pulmonary disease. A pulmonary function of less than 35% of predicted is associated with a protracted postoperative course with an increased risk of ventilation dependency.

Patients with Duchenne's muscular dystrophy and Friedreich’s ataxia should have a preoperative cardiac assessment as well.

Treatment

Nonoperative Treatment

Minor neuromuscular curves less than 20º can be observed. When the curve reaches 20º and progression is noted, treatment should be considered.

Bracing

Most neuromuscular curves cannot be definitively treated with a brace, but braces may be used to slow the progression and improve sitting posture in young patients with flexible curves.15,16 Traditional braces such as the Milwaukee are contraindicated because many neuromuscular patients have poor motor control, limited respiratory function, and poor nutritional status due to limited gastric motility.

Surgery

Although curve size greater than 50º with rapid progression is an indication for surgery, the most important indication for surgery is whether the patient experiences a functional deficit as a result of progressive scoliosis. Maintaining ambulation, comfortable sitting independence, positioning for use of the upper extremities, and/or preventing cardiopulmonary compromise are considered justifiable reasons for surgery.

Many patients suffering from neuromuscular scoliosis have associated medical problems (seizure disorders, restrictive lung disease, cor pulmonale, cardiomyopathy, and poor nutritional status) that put them at high risk for operative complications.¹⁷

Attaining good spinal balance in the coronal and sagittal planes is important because these patients do not have compensatory mechanisms (muscle tone, intact proprioception) to rebalance themselves.

Posterior Instrumentation and Fusion
In contrast to idiopathic scoliosis, selective spinal fusion should be avoided in neuromuscular scoliosis because the underlying neuromuscular condition will continue to exert force on the non-fused segment, creating new deformities. Due to the associated kyphosis and pelvic obliquity, the levels of fusion are usually extended past the Cobb to prevent junctional kyphosis (usually to the first lordotic segment both proximally and distally).¹⁸

The standard posterior instrumentation method for most neuromuscular patients is the Luque method that uses sublaminar wires.³ This technique is beneficial because it provides fixation at every level, which protects the weakened bone from failure and prevents the need for postoperative immobilization. A precontoured unit rod can be added to allow greater control of the spine and better correction of pelvic obliquity.^4,5,6 The use of a multihook instrumentation system is also an option, using the Cotrel-Dubousset system.⁷ Pedicle screws can provide enough correction to allow for single-stage posterior spinal fusion and instrumentation without the need for anterior spinal release.¹⁹

Fusion across the lumbosacral junction is required in neuromuscular scoliosis when the curve is greater than 40º and pelvic obliquity is greater than 10º. The Luque-Galveston technique involves fusion from T2 to the posterior superior iliac spine.²⁰ However, it has been shown that the unit rod is more effective in correcting pelvic obliquity and spinal deformity.²¹ A maximal width segmental pelvic fixation has been shown to be effective for severe pelvic obliquity.²²

Anterior Spinal Instrumentation
Anterior spinal instrumentation without posterior fusion is rarely indicated in neuromuscular scoliosis. However, it may be used in patients with contraindications to posterior spinal fusion (chronic wound infection) and small flexible curves less than 70º with no need to extend fusion to the pelvis.²⁷

Anterior Spinal Release and Fusion
Anterior spinal release and fusion are indicated in neuromuscular scoliosis patients with large rigid curves, significant pelvic obliquity, thoracic kyphosis greater than 60º-70º, skeletal immaturity (to prevent the crankshaft phenomenon), and increased risked of non-union (patients with myelomeningocele with deficient posterior spinal elements).

Bone Graft
An allograft is an accepted bone grafting substitute for spinal fusion in neuromuscular scoliosis because the pelvis in a patient with neuromuscular scoliosis tends to be small.²³

Severe Rigid Neuromuscular Scoliosis
Some neuromuscular scoliosis curves are so rigid that they require spinal osteotomies, vertebrectomies, or even kyphectomies.

Spinal Cord Monitoring

In patients with neuromuscular scoliosis, spinal monitoring with somatosensory evoked potential or motor evoked potential is crucial. When this is not possible, the Stagnara wake-up test may be used.^29,30

Outcome

• Postoperative and long-term follow-up indicate that L5 fusion can correct scoliosis and pelvic obliquity comparable to sacral fusions.³¹
• Anterior spinal surgery has been associated with an increased morbidity especially in patients with neuromuscular disease.²⁴
• About half of myelomeningocele patients with posterior spinal fusion will develop a deep posterior spinal infection that may necessitate hardware removal.^10,19,25,26
• Complications in staged anterior and posterior surgery have been found to be higher than same-day front and back surgery.²⁸

Complications

Intra-operative Complications

• Blood loss
• Neurologic injury
• Vascular injury
• Direct trauma
• Ischemia
• Pneumothorax

Post-operative Complications

• Infection
• Hematoma
• Neurologic deterioration
• Pneumonia
• Ileus
• Pulmonary embolism

Delayed Complications

• Pseudarthrosis
• Failed instrumentation
• Loss of correction
• Adjacent level degeneration
• Back pain

Pearls and Pitfalls

• Kyphoscoliosis is synonymous with neuromuscular scoliosis, compared with lordoscoliosis seen with idiopathic scoliosis.
• Pelvic obliquity is pathognomonic for neuromuscular scoliosis.
• Spinal deformity in patients with neuromuscular scoliosis tends to occur early and is rapidly progressive.
• Surgical management of patients with neuromuscular scoliosis is associated with greater risk because these patients tend to have associated medical problems.
• Spinal fixation is difficult because bone is weakened by disuse, osteopenia, and antiepileptic drugs.

Controversy

• The indication for surgery in neuromuscular patients remains controversial.⁸
• When both anterior spinal release and fusion are required, the optimum timing of the anterior surgery is controversial.²⁸

References

1. Rosenthal RK, Levine DB, McCarver CL. The occurrence of scoliosis in cerebral palsy. Dev Med Child Neurol. 1974;16(5):664-7.
2. Mehta S, Betz RR, Mulcahey MJ, et al. Effect of bracing on paralytic scoliosis secondary to spinal cord injury. J Spinal Cord Med. 2004;27(Suppl 1):S88-92.
3. Luque E. Segmental spinal instrumentation for the correction of scoliosis. Clin. Orthop. 1982;163:192-198.
4. Bell D, Moseley C, Koreska J. Unit rod segmental spinal instrumentation in the management of patients with progressive neuromuscular spinal deformity. Spine. 1989;14:1301-1307.
5. Bulman W, Dormans J, Ecker M, et al. Posterior spinal fusion for scoliosis in patients with cerebral palsy: A comparison of Luque rod and unit rod instrumentation. J. Pediatr. Orthop. 1996;16:314-323.
6. Maloney WJ, Rinsky LA, Gamble JG. Simultaneous correction of pelvic obliquity, frontal plane, and sagittal plane deformities in neuromuscular scoliosis using a unit rod with segmental sublaminar wires: A preliminary report. J. Pediatr. Orthop. 1990;10:742-749.
7. Neustadt JB, Shuflebarger HL, Cammisa FP. Spinal fusions to the pelvis augmented by Cotrel-Dubousset instrumentation for neuromuscular scoliosis. J. Pediatr. Orthop. 1992;12:465-469.
8. Lonstein J, Akbarnia B. Operative treatment of spinal deformities in patients with
   cerebral palsy or mental retardation. J Bone Joint Surg Am. 1983;65:43--55.
9. Hart D, McDonald C. Spinal deformity in progressive neuromuscular disease. Phys Med Rehab Clin North Am. 1998;9(1):213-32.
10. Lindseth RE. Spine deformity in myelomeningocele. Instr Course Lect. 1991;40:276.
11. Majd ME, Muldowny DS, Holt RT. Natural history of scoliosis in the institutionalized adult cerebral palsy population. Spine. 1997;22:1416--1466.
12. Oda T, Shimizu N, Yonenobu K, et al. Longitudinal study of spinal deformity in Duchenne muscular dystrophy. J Pediatr Orthop. 1993;13:478--188.
13. McDonald C, Abresch T, Carter G, et al. Profiles of neuromuscular diseases: Becker muscular dystrophy. Am J Phys Med Rehabil. 1995;74:S93--103.
14. Horstman H, Boyer B. Progression of scoliosis in cerebral palsy patients after skeletal maturity. Dev Med Child Neurol. 1984;26:261.
15. Miller A, Temple T, Miller F. Impact of orthoses on the rate of scoliosis progression in children with cerebral palsy. J Pediatr Orthop. 1996;16(3):332--335.
16. Olafsson Y, Sarast H, et al. Brace treatment in neuromuscular spine deformity. J Pediatr Orthop. 1999;19(3):376--9.
17. Winter S. Preoperative assessment of the child with neuromuscular scoliosis. Orthop Clin North Am. 1994;25:239--245.
18. Lee GA, Betz RR Clements DH 3rd, Huss GK. Proximal kyphosis after posterior spinal fusion in patients with idiopathic scoliosis. Spine. 1999;24(8):795--9.
19. McMaster MJ. Anterior and posterior instrumentation and fusion of thoracolumbar scoliosis due to myelomeningocele. J Bone Joint Surg Br. 1987;69:20-5.
20. Gau Y, Lonstein J, Winter R, et al. Luque-Galveston procedure for correction and stabilization of neuromuscular scoliosis and pelvic obliquity: a review of 68 patients. J Spinal Disord. 1991;4:399--410.
21. Bulman W, Dormans J, Ecker M, et al. Posterior spinal fusion for scoliosis in patients with cerebral palsy: a comparison of Luque rod and Unit Rod instrumentation. J Pediatr Orthop. 1996;16:314--323.
22. Arlet V, Marchesi D, Papin P, Aebi M. The ’MW’ sacropelvic construct: an enhanced fixation of the lumbosacral junction in neuromuscular pelvic obliquity. Eur Spine J. 1999;8(3):229--31.
23. Yazici M, Asher M. Freeze-dried allograft for posterior spinal fusion in patients with neuromuscular spinal deformities. Spine. 1997;22:1467--1471.
24. Grossfeld S, Winter B, et al. Complications of anterior spinal surgery in children.
    J Pediatr Orthop. 1997;17(1):89--95.
25. Mazur J, Melelaus MB, Dicksen DR, et al. Efficacy of surgical management for scoliosis in myelomeningocele: Correction of deformity and alteration of functional status. J Pediatr Orthop. 1986;6:568-75.
26. Osebold WR, Mayfield JK, Winter RB, et al. Surgical treatment of the paralytic scoliosis associated with myelomeningocele. J Bone Joint Surg Am. 1982;64:841-56.
27. Sponseller PD, Young AT et al. Anterior only fusion for scoliosis in patients with myelomeningocele. Clin Orthop. 1999;364:117--24.
28. Ferguson RL, Hansen MM, Nicholas DA, Allen BL Jr. Same-day versus staged anterior-posterior spinal surgery in a neuromuscular scoliosis population: the evaluation of medical complications. J Pediatr Orthop. 1996;16(3):293--303.
29. Hall JE, Levine CR, Sudhir KG. Intraoperative awakening to monitor spinal cord function during Harrington instrumentation and fusion: description of procedure and report of three cases. J Bone Joint Surg Am. 1978;60:533--536.
30. Wilson-Holden TJ, Padberg AM, Lenke LG, Larson BJ, Bridwell KH, Bassett GS. Efficacy of intraoperative monitoring for pediatric patients with spinal cord pathology undergoing spinal deformity surgery. Spine. 1999;24(16):1685--92.
31. McCall RE, Hayes B. Long-term Outcome in Neuromuscular Scoliosis Fused Only to Lumbar 5. Spine. 2005;30(18):2056-2060.