24 Neuromuscular Scoliosis Jean A. Ouellet, Vincent Arlet Core Messages ✔ Kyphoscoliosis is a synonym for neuromuscular scoliosis, in contrast to lordoscoliosis, which is a synonym for idiopathic scoliosis ✔ Hyperlordosis is also seen in neuromuscular scoliosis ✔ Pelvic obliquity is pathognomonic for neuro- muscular scoliosis ✔ Spinal deformities in neuromuscular patients tend to be severe and progressive in both coro- nal and sagittal planes ✔ Surgical management of patients with neuro- muscular scoliosis is associated with greater morbidity as they can have severe comorbid medical problems ✔ Duchenne muscular dystrophy and Friedreich’s ataxia should always have a preoperative car- diac assessment ✔ Preoperative pulmonary function of less than 35% of the predicted value indicates postopera- tive ventilatory support and dependency, which may put the surgical indications in question ✔ Maximizing hemostasis with adjuvant con- trolled hypotension, cell savers, hemostatic agents and excellent vascular access is impera- tive since intraoperative bleeding can be signif- icant (up to two times blood volume) ✔ Spinal fixation may be complicated and prone to failure since bone is weakened by disuse, osteopenia and antiepileptic drugs ✔ Achieving spinal balance in both the coronal and sagittal planes is even more critical as patients with neuromuscular scoliosis typically do not have the innate ability to compensate and balance themselves postoperatively ✔ Fusion often extends to the pelvis; thus a good understanding of different pelvic-lumbosacral fixations is mandatory ✔ Never extend a fusion down to the pelvis in a patient relying on a mobile lumbosacral junc- tion for his or her ambulation, even in the pres- ence of pelvic obliquity ✔ If the curve <40° and the pelvic obliquity < 10°, one can stop the fusion at L5; if these are greater then the fusion should be extended to the pelvis Epidemiology Neuromuscular scoliosis embodies a heterogeneous group of patients Scoliosis in the presence of a neuromuscular disorder (NMD) behaves entirely differently from the more predictable idiopathic scoliosis. Depending on the underlying NMD, the prevalence of scoliosis is also different. Having a better understanding of these disorders facilitates the management of their associated spinal deformities ( Table 1). Treatment must be individualized for each underlying diagnosis One must appreciate that the heading of neuromuscular scoliosis encom- passes a large variety of different NMD pathologies. These disorders can present either early or later in life. They can be acquired by means of postinfectious or post-traumatic events, or they can be genetic disorders affecting genes that code for the proteins in nerve cells or in muscle cells, leading to malfunction of the neurological or muscular systems. They can also be secondary to brain or spinal cord insults or disease. The majority of these disorders present in different sever- Spinal Deformities and Malformations Section 663 a b cd e f Case Introduction A 4-year-old boy with Duchenne muscular dystrophy had been followed at the neuromuscular clinic at regular intervals to monitor respiratory status and general development. On initial screening, spine X-ray did not demon- strate any spinal deformity (a, b). At the age of 6, spinal asymmetry was noted and a 10° scoliosis documented. By the age of 10, the curve had pro- gressed to 48° ( c). Respiratory functions were 35% of expected and deemed amenable to spinal surgery with moderate perioperative risk. The patient had a classic segmental posterior spinal fusion using sublaminar wiring from T2 to L5 ( d). A decision was made to fuse to L5 and not fuse to the pelvis considering that his pelvic obliquity was minimal <10° and flexi- ble ( e, f). By doing so the risk of pseudoarthrosis across the lumbosacral junction was minimized. Being a male and non-ambulator the fusion could have been extended to the pelvis to prevent the possibility of progressive pelvic obliquity. In girls that perform self-catherization, fusing to the pelvis often leads to loss of independence of self-care. The second contentious decision was that no anterior spinal fusion was done due to the fear that he would not tolerate the extended surgery. Fusing the spine at such a young age poses a risk of the patient developing a crankshaft deformity; however, considering that he had passed his peak growth velocity, this risk was mini- mal. Furthermore any decisions must take into account his truncated life expectancy. Of note is that the rods were inappropriately contoured lack- ing lumbar lordosis to achieve an adequate sagittal balance. Table 1. Characteristics of neuromuscular disorders associated with scoliosis [15, 34, 47] Disease (incidence) Onset (years) Inheritance Life expectancy (years) Presentation Progression of weakness Loss of ambula- tion (years) Muscular dystrophies Duchenne (1:4000 male births) 1.5–4 XR 20±4 Proximal muscle weakness, lower weaker than upper limbs, extensor weaker than flexor, muscles of heart and respiratory system Rapid decline from 5 to 13 years, slower after 14 10 ±2.5 Becker (4:100 000 male births) 8.5±8.5 XR 23–89 Distribution similar to Duchenne Slow decline 25–58 664 Section Spinal Deformities and Malformations Table 1. (Cont.) Disease (incidence) Onset (years) Inheritance Life expectancy (years) Presentation Progression of weakness Loss of ambula- tion (years) Muscular dystrophies Limb girdle (incidence cannot be estimated) 9±4 AR (expAD) variable distribution similar to Duchenne and Becker except no difference of extensor and flexor rapid loss 75% by age 20 Myotonic (AKA Steinert’s) (1:20000 births) 23±13 AD variable (dependent on arrhyth- mias) facial weakness notice first, ptosis, generalized weakness of voluntary muscles of limbs, distal muscle weakness, and the neck, facial, and diaphragm muscles, and intercos- tals. Develops heart blocks, unable to release grasp slow loss late in life if ever Congenital myotonic at birth AR variable (% neona- tal death) severe weakness, floppy baby, require ventilation and nutrition supplement as infant, moderate mental retardation may never reach ambula- tion Arthrogryposis (1:3 000 births) at birth non-genetic fetal akine- sia, 30% AR normal (50% neo- natal death when CNS) focal weakness in presence of severe joint contractures: classic hands, wrists, elbows, shoulders, hips, feet and knees. Severe cases, all joints including jaw and spine static; may pro- gress with dis- use, atrophy may be present, and muscles or muscle groups may be absent variable spinal muscular atrophy (1 : 6000 births) Type I (acute infantile, acute Werdnig-Hoff- mann disease) 0–0.5 AR 1.5 (50 % die before 2years) severe generalized muscle weak- ness leading to feeding and breath- ing failures, unable to sit never ambulate Type II (chronic Werdnig-Hoff- mann diseases) 2 30–40 proximal muscle weakness, lower weaker than upper limbs, extensor weaker than flexor, sits but diffi- culty walking if able progression variable early loss Type III (Kugel- berg-Welander diseases) 23±19 normal proximal muscle weakness, no dif- ference between lower and upper or flexor and extensor slow loss very late if any Poliomyelitis (prevalence in 2003: 623 cases worldwide) variable acquired (Nigeria, India, Paki- stan, Afgha- nistan, Egypt) normal (may require respiratory support) prodrome: fever 5–7 days before headache, stiff neck, paraspinal muscle weakness, asymmetrical peripheral weakness (only on one side or worse on one side), distribu- tion depends on level of cord involvement, abnormal sensations with hypersensitivity rapid onset progresses to paralysis, per- manent or tran- sient with pos- sible mild delayed regres- sion variable depen- dent on severity, subclini- cal, non- paralytic, paralytic Hereditary motor sensory neuropathy Charcot-Marie- Tooth (1:2 500 births) 13±14 AD relatively normal distal muscle weakness, no differ- ence upper vs lower, nor flexor vs extensors slow loss later if any Cerebral palsy (2:1000 births) at birth acquired brain insult in utero/peri- natally, post- infectious variable (dependent on mobility; non-sitter: 30; sitter: 46; ambula- tor: 62) spastic (50%): stiff, difficult move- ment dyskinetic/athetoid (20%): involun- tary uncontrolled movement ataxic (rare): poor coordination and balance mixed (30%): combination of these types hypotonia may develop into spasticity variable Spinocerebellar dysfunction Friedreich’s ataxia (1:22000 births) 10±5 AR early adulthood 38 ±14 (cardiac) initially difficulty walking, ataxia, then spreading to arms then trunk, muscle weakness, muscle wasting: feet, leg, hands, loss of sensation over time, nystagmus, cardiomyop- athy, myocardial fibrosis slow progres- sive 15–20 years after diagnosis Neuromuscular Scoliosis Chapter 24 665 ities: from mild, to moderate, to severe forms. They may result in minimal clini- cal manifestation or they can result in lethal disease in early infancy. An overview of these disorders with their clinical presentations, their incidence and their functional impact is given in Table 1. Disease Specific Spinal Deformity As part of a review of 547 individuals with different NMDs, the Rehabilitation Research and Training Center (RRTC/NMD) found that the overall incidence of Spinal deformity is frequent and severe in rapidly progressive NMD spinal deformity was elevated (60–80%) in patients with rapidly progressive NMD who presented before skeletal maturity [41], while in slowly progressive NMD the incidence of scoliosis was relatively low (only 32%). In the patients with rapidly progressive NMD, the incidence and severity of the scoliosis increased with disease duration and years of wheelchair dependency, with a high incidence of pulmonary complications and decreased pulmonary function. In contrast, in patients with slowly progressive NMD, the presence of spinal deformity showed no relationship between disease duration and length of wheelchair dependency. The scoliosis of these patients was often mild to moderate and usually non-pro- gressive. There was, however, a significant association between the number of pulmonary complications and disease duration in those patients with spinal deformity who also had significantly lower vital capacities. One must keep in mind that these are general guidelines and do not imply a cause to effect relation- ship between specific disease and the development of scoliosis. Duchenne patients are likely to develop scoliosis For example, in Duchenne muscular dystrophy (DMD), there is a progressive increase in incidence of scoliosis up to the age of 20 years ( Case Introduction). The incidence increases significantly once patients are wheelchair dependent, especially after 3 years, when the incidence is close to 60%. Thirty-five percent of patients have spinal deformity before the age of 8 years, and 90% do so by the age of 20 years [15]. The incidence increases greatly between the ages of 13 and 15 years, which correspond closely with the adolescent growth spurt in boys. In contrast, in patients with Becker’s muscular dystrophy,only13%hadscoli- osis with mild non-progressive curves. Patients with hereditary motor sensory neuropathy (HMSN, Charcot-Marie-Tooth disease) had a 25% incidence of spi- nal deformity, of whom 15% had scoliosis and 10% had kyphoscoliosis. In patients with Friedreich’s ataxia, the incidence of scoliosis was almost 100%, compared to only 32% in those with other types of hereditary spinal cerebellar ataxia (HSCA). Patients with infantile onset spinal muscular atrophy (SMA) had a 78% incidence of scoliosis while juveniles and adults with SMA onset had only 8% incidence. Spinal deformity in the congenital myopathies occurred primarily in the individuals with congenital muscular dystrophy (36%). Thirty-five percent of patients with facioscapulohumeral dystrophy had spinal deformity, of whom 15% had scoliosis alone. The incidence of spinal deformity in limb girdle syn- drome also depended on the type. Individuals with the childhood onset type had a 44% incidence while those with the late onset and pelvofemoral types had only a 6% incidence. There was a marked difference in the incidence of spinal defor- mity between congenital myotonic muscular dystrophy (MMD) and non-con- genital MMD. Forty-seven percent of the former had scoliosis as compared to 15% of the latter. Ninety percent of myelodys- plasia patients with a T10 level will develop a spinal deformity With respect to patients with myelodysplasia, the prevalence will vary depending on their functional level: 90% of patients with a complete T10 level will develop a coronal or sagittal spinal deformity, while only 5% of patients with an L5 level will develop a spinal deformity [20]. The overall incidence of spinal deformity varies depending on the underlying NMD, but it also varies according to the severity of the underlying NMD 666 Section Spinal Deformities and Malformations Table 2. Prevalence of spinal deformities in neuromuscular diseases Diagnosis Percentage a Cerebral palsy 25 Poliomyelitis 17–80 Myelodysplasia 60 Spinal muscular atrophy 67 Friedreich’s ataxia 80 Duchenne muscular dystrophy 90 Spinal cord injury (traumatic before 10 years of age) 100 a Based on data by J.E. Lonstein, Department of Orthopedics, University of Minnesota, Twin Cities Spine Center, Minneapolis (Table 2). In general, the greater the neuromuscular involvement, the greater the likelihood of having a spinal deformity and the greater the deformity will be. Pathogenesis The pathophysiology of neurogenic spinal deformities remains unclear. It seems logical to assume that the “collapsing kyphoscoliosis” is secondary to muscle weakness and yet the same deformity is seen in patients with spasticity. The clas- sical spinal deformities encountered in NMD consist of: scoliosis kyphosis kyphoscoliosis lumbar hyperlordosis pelvic obliquity Pelvic obliquity is an associated spinal deformity Pelvic obliquity should be considered as an associated “spinal” neurogenic deformity. All of these deformities canbe present with any of the different NMDs, making it difficult to draw any conclusion about the pathogenesis of neuromus- cular scoliosis. Furthermore there is no association between etiology, pattern of weakness, and curve pattern. There are factors that influence the development of certain deformities. For example, the development of scoliosis is influenced by the following factors: age of onset of NMD ambulation status severity and rapidity of the progression of the weakness This is particularly true for patients with Duchenne muscular dystrophy. Close to 90% of them will develop scoliosis as their weakness progresses quickly, and it occurs prior to cessation of growth coupled with loss of ambulation at an early age. However, these factors do not always lead to a deformity, such as in patients with amyotrophic lateral sclerosis, which is a very rapid progressive NMD and yet only 1% develop scoliosis. Classification The classic patient we think of having neuromuscular scoliosis has either cerebral palsy (upper motor neuron lesions) or Duchenne muscular dystrophy (peripheral muscular disease) [4]. These two etiologies are representative of the two main types of neuromuscular scoliosis. The Scoliosis Research Society has classified neuromuscular scoliosis into neuropathic types and myopathic types ( Table 3 ). Neuromuscular Scoliosis Chapter 24 667 Table 3. Classification of neuromuscular scoliosis Neuropathic conditions Myopathic conditions Upper motor neuron cerebral palsy syringomyelia spinal cord injury Lower motor neuron poliomyelitis spinal muscular atrophy Mixed upper and lower motor neuron myelodysplasia (spina bifida) spinal trauma Spinocerebellar dysfunction Friedreich’s ataxia Hereditary motor sensory neuropathy Charcot-Marie-Tooth Muscular dystrophy Duchenne and Becker limb girdle facioscapulohumeral myotonic dystrophy Arthrogryposis Congenital myopathies nemaline central core disease Lonstein et al. [22] classified the curve patterns of neuromuscular scoliosis in patients with cerebral palsy and mental retardations into two large groups each subdivided into two subgroups ( Fig. 1). The difference between the groups is the presence (G-II) or absence (G-I) of pelvic obliquity, which has a clinical bearing as to whether to include the pelvis in the spinal fusion. Figure 1. Neuromuscular curve classification Group I: double thoracic and lumbar curves, little pelvic obliquity, patient in balance. a Thoracic lumbar curve in balance; b thoracic greater than lumbar curve, unbalanced. Group II: large lumbar or thoracolumbar curves, severe pelvic obliq- uity, patient out of balance. c Short fractional curve above sacrum; d extension of lumbar curve in sacrum (According to Lonstein et al. [22]). 668 Section Spinal Deformities and Malformations Clinical Presentation History As in any ailment, obtaining a detailed history is fundamental in the establish- ment of the correct diagnosis of scoliosis. A thorough history should include: perinatal history development history family history A family history is required to assess the risk of a known etiology for the patient’s spinal deformity. Clues suggestive for neuromuscular scoliosis are: birth anoxia delayed developmental milestone acquired or familial neuropathies and/or myopathies early onset (less than 7 years old) painful scoliosis Detailed perinatal history and family history is warranted if neuromuscular scoliosis is suspected The patient should be asked about maternal diabetes, specific bowel and bladder functions, and muscle endurance since these insignificant details can lead to a diagnosis of sacral agenesis or then again to that of a tethered cord. Subjective complaints of patchy numbness and weakness must be elicited as well as symp- toms consistent with radiculopathy, myelopathy, or recurrent headaches, which mayallbesymptomsofasyringomyelia( Table 4). Table 4. Red flags for neuromuscular scoliosis History: early onset scoliosis: early, less than 7 years of age painful scoliosis headache sensory or motor disturbances bowel and bladder dysfunction developmental delay, mental retardation Physical examination: Head & neck: flaccid facies poor head control Skin: neuroectodermal lesions: caf´eaulaitspots spinal dysraphism: hairy patch, sacral dimples, midline birthmark Spine: long collapsing scoliosis pelvic obliquity kyphoscoliosis lack of rotation Neurology: spasticity muscle weakness, proximal girdle + Gower peroneal muscular weakness long track signs: clonus, Babinsky’s, hyperreflexia hypotonia, hyporeflexia patchy paresthesia Musculoskeletal: limb atrophy, different feet size cavus feet upper extremity posturing during running loss of sitting balance Charcot joints non-ambulators Neuromuscular Scoliosis Chapter 24 669 Physical Examination Skin Thedermismustbeinspectedforskinlesionssuchascaf´eaulaitspotsor axil- lary freckles as these are associated with neurofibromatosis, which can have intradural neuromas. Other neurocutaneous skin markings such as hairy patches ( Fig. 2) or midline nevi (or vascular lesion) can also be superficial clues to intradural pathologies. Spine Coronal imbalance is frequent in neuromuscular scoliosis Neuromuscular scoliosis resembles a kyphoscoliotic deformity, in contrast to the lordoscoliosis found in adolescent idiopathic scoliosis. Ky phosis is frequently found as an associated spinal deformity in the neuromuscular patient as the majority of them have “collapsing spine” secondary to muscular weakness or deficient trunk control ( Case Study 1). Patients must be examined for both defor- mities in the sitting and supine positions, giving us an immediate insight into the overall rigidity of both deformities. Of note, hyperlordosis can also be seen in neuromuscular scoliosis, leading to inability to sit properly. Sagittal imbalance with apical kyphosis is also frequent The combination of pelvic obliquity and scoliosis tends to lead to spinal imbalance, resulting in abnormal pressure points. Patients with neuromuscular scoliosis can develop pressure sores on the sacrum, the ischia, and the greater trochanter and these should be looked for. a b c d Figure 2. Clinical clues to neuromuscular scoliosis a Eleven-year-old boy, idiopathic-like curve pattern, asymptomatic. On examination unilateral cavus foot with calf atro- phy is noted. b The patient presents with a myopathic scoliosis due to Charcot-Marie-Tooth disease. c Seven-year-old girl, right thoracic curve, with overt neuroectodermal marker – hairy patch. d The patient is diagnosed with diastematomye- lia and tethered cord. 670 Section Spinal Deformities and Malformations ab c d ef g Case Study 1 A 12-year-old boy with congenital myopathy (a) presented at our neuromuscular clinic with his older brother (b), who was also diagnosed with neuromuscular scoliosis. His brother had undergone a selective thoracic posterior spinal fusion with Harrington rod 15 years earlier ( c). Over time the brother developed additional deformity above and below and crankshaft deformity across the instrumented segment. The main concern of the younger brother was not to end up like his older brother. The patient has severe coronal imbalance with a significant pelvic obliquity ( d, e). Surgical manage- ment must address both the long classic C-shape neuromuscular scoliosis and the pelvic obliquity. The primary goal is to achieve coronal and sagittal balance. Despite the relatively rigid upper thoracic deformity, correction was achieved by posterior alone spinal surgery with a solid pelvic fixation comprising MW construct, pedicle screws above and below and apical sublaminar wire to maximize apical translation ( f, g). The MW “segmental pelvic fixation” (see Fig. 5) allows (if needed) for further pelvic correction by levering on the iliosacral screws in the up or down hemipelvis depending on residual obliquity even after the cantilever maneuver has been done. Neuromuscular Scoliosis Chapter 24 671 Pelvis and Hips Hip contractures will influence treatment From a musculoskeletal examination point of view, one must assess the skeletal appendages as well as the spine. A detailed examination of the hips particularly looking for hip contracture is crucial as they influence sitting balance and in par- ticular can induce pelvic obliquity ( Case Study 1). As there are many patients with neuromuscular scoliosis who are wheelchair dependent, one must pay par- ticular attention to the pelvis and its orientation in both the coronal (obliquity) and sagittal plane (anteversion/retroversion). If pelvic obliquity is present, one should assess whether its origin is: suprapelvic intrapelvic infrapelvic [13] Pelvic obliquity is pathognomonic for neuromuscular scoliosis Suprapelvic obliquity is secondary to the spinal deformity itself. The scoliosis drives the pelvis in its obliquity. Dubousset saw the pelvis as the 6th lumbar ver- tebra and the pelvis being a simple extension of the scoliotic deformity resulting in pelvic obliquity. In contrast, infrapelvic obliquity is secondary to hip contrac- tures which result in pelvic obliquity. The contractures which drive the pelvic obliquity tend to be abduction or adduction hip contractures. When both are present in opposite hips one talks of windswept deformity of the hips, which typ- ically results in significant pelvic obliquity. NMD patients often develop hip flexion contractures In addition, as the majority of these patients are wheelchair dependent, they develop hip flexion contractures. These may induce fixed or flexible sagittal spi- nal deformity in the form of lumbar hyperlordosis. Orientation of the pelvis and lumbar lordosis needs to be assessed as an anteverted pelvis or compensatory hyperlordosis can indicate severe hip flexion contracture. These postoperatively maybecomemuchmoreapparentasthepatientsarenolongerabletocompen- sate with their flexible lumbar spine. To differentiate between supra- and infrapelvic obliquity, the patient is placed prone at the end of an examining table with the hips flexed over the edge of the table (negating the flexion hip contractures). Then by abducting or adducting the hips, the pelvis can be leveled in the infrapelvic obliquity, while for the suprapel- vic obliquity the pelvis cannot be leveled by changing the position of the hips. An understanding of pelvic obliquity is a key to treatment Intrapelvic obliquity is secondary to morphological changesof the hemipelvi- ses. This can be seen in asymmetrical myelomeningocele as the weaker side develops less, resulting in bony architectural changes leading to ischial and ilium hypoplasia. Pelvic X-rays are the only way to identify such pelvic obliquity. Ambulatory Status and Mode of Ambulation It is not enough to know if the patient is a: walker sitter (wheelchair bound) non-sitter Mode of ambulation determines the extent of instrumented fusion In the walker, one must determine gait pattern and mode of ambulation. Certain patients (myelodysplasia) need a mobile lumbosacral junction to ambulate as they rely on pelvic thrust to propel their lower extremities to ambulate. Extend- ing the fusion to the pelvis in this subpopulation would take away their ability to ambulate. Even in the wheelchair-bound patient, a mobile lumbosacral junction may be needed to perform self-catheterization. Thus, the decision to extend the fusion to the pelvis must be done with careful consideration. 672 Section Spinal Deformities and Malformations . Thirty-five percent of patients have spinal deformity before the age of 8 years, and 90% do so by the age of 20 years [15]. The incidence increases greatly between the ages of 13 and 15 years, which. example, the development of scoliosis is influenced by the following factors: age of onset of NMD ambulation status severity and rapidity of the progression of the weakness This is particularly true. NMD, the prevalence of scoliosis is also different. Having a better understanding of these disorders facilitates the management of their associated spinal deformities ( Table 1). Treatment must be individualized