Current concepts review: Low-vs high-tone neuromuscular spinal deformities: An evolving distinction with clinical implications

Abstract

Background

Neuromuscular scoliosis (NMS) was historically classified into two groups as neuropathic and myopathic, which offers limited benefit beyond describing the underlying pathology. More recently, NMS is being classified according to changes in muscle tone, which more accurately characterizes presenting features, and also helps emphasize the critical differences in management.

Clinical Presentation

High-tone NMS, with cerebral palsy (CP) as a typical example, is characterized by spasticity, rigidity, and often reduced flexibility. Low-tone NMS, as in spinal muscular atrophy (SMA) and muscular dystrophy presents with hypotonia and truncal weakness, leading to more flexible, long curves often with significant kyphosis. High burden of medical comorbidities is common in both groups, while low-tone patients carry a higher risk of respiratory failure secondary to severe muscle weakness and cardiac involvement in myopathies and muscular dystrophies.

Management

Successful management depends on careful evaluation of muscle tone, and tailoring the treatment accordingly. Multidisciplinary care is essential, and preoperatively all patients should be evaluated for possible respiratory problems and nutritional optimization. Muscular dystrophies and myopathic conditions require careful cardiac evaluation. Principles of surgical treatment may be similar for both low-tone and high-tone patients, but characteristics of the underlying disease can affect the details of treatment.

Conclusion

Surgery can be performed safely and provide significant improvements in quality of life in NMS. Recent evidence suggests that surgery may also decrease mortality and help preserve pulmonary function. Distinguishing low-from high-tone NMS provides a clinically meaningful framework.

Introduction

Neuromuscular scoliosis (NMS) is a form of spinal deformity occurring secondary to a underlying neuromuscular condition. ¹ These underlying conditions are various, and have historically been classified under two major groups: neuropathic and myopathic. ² This classification offers very limited benefit beyond describing the underlying pathology and has not substantially contributed to guiding treatment decisions or defining distinct clinical characteristics. More recently, another classification has emerged based on alterations in muscle tone, distinguishing low-tone from high-tone disorders, and this distinction is increasingly gaining recognition. ³ Different neuromuscular disorders can alter muscle activity and tonus in different directions: high-tone disorders (such as cerebral palsy-CP, spinal cord injuries and Rett syndrome, the latter two after the early stages) cause hypertonia and spasticity, while low-tone disorders (such as spinal muscular atrophy-SMA, muscular dystrophies, congenital myopathies and poliomyelitis) result in hypotonia and generalized muscle weakness. Spinal cord injuries and Rett syndrome may exhibit changes in muscle tone throughout the course of the disease. Both conditions are characterized by hypotonia in the early stages, which may gradually progress to hypertonia by the time scoliosis requires surgical intervention.^4,5

NMS can present at any age in these patients, caused mainly by muscular imbalance secondary to the aforementioned underlying disorders. Both hypotonia and hypertonia of the trunk muscles can play a role in this imbalance. ⁶ Progression of the deformity is the result of both persistent or worsening muscular imbalance and anatomic deformity caused by asymmetric loading. ²

Recent studies have started recognizing the importance of differentiating high-tone from low-tone neuromuscular scoliosis, as this fundamental distinction shapes deformity morphology and has important implications for treatment.^3,7–9 The distinction between high- and low-tone disorders is not sharply defined in the literature; however, this classification shows promise in providing a framework for accurately characterizing presenting features, guiding treatment strategies, safely navigating the perioperative period and assessing outcomes. This review aims to consolidate and summarize the current literature on the etiology, natural history, clinical evaluation, and management of neuromuscular scoliosis, with particular emphasis on the distinguishing features of low-tone versus high-tone deformities.

Clinical Presentation

NMS differs from idiopathic scoliosis with its often earlier onset, rapid and relentless progression, and higher risk of progression after skeletal maturity. ⁶ Neuromuscular curves are also morphologically different from their idiopathic counterparts as they are more likely to be long, sweeping, C-shaped curves that extend into the pelvis, although S-shaped curves are also seen (Figure 1). ² The difference between idiopathic and neuromuscular spinal deformities stems from the underlying pathologic mechanisms. Although not proven to date, it is widely accepted that because of the underlying neuromuscular disorder, body cannot produce the compensatory forces to bring the head over the pelvis and maintain neutral alignment.

Figure 1.

15-year old male patient with CP, functional level is GMFCS V. Preoperative (A) radiographs demonstrate an S-shaped curve with 70° magnitude, and significant coronal imbalance. The curve reduced to 16° with traction (B). Posterior spinal fusion was done from T3 to pelvis, and S2AI screws were used for pelvic fixation. Excellent correction was achieved, and postoperative radiographs (C) show good coronal and sagittal balance.

Low-tone NMS shares the general characteristics of neuromuscular curves as it is often long and sweeping, C-shaped, accompanied by pelvic obliquity, and rapidly progressive. Distinguishing features include kyphosis accompanying the scoliosis, as frequently encountered in SMA (Figure 2), along with progressive respiratory decline resulting from weak intercostal muscles and a collapsing thoracic cage, a phenomenon often referred to as the ‘parasol’ deformity.^7,10,11 In contrast, high-tone deformities tend to demonstrate reduced flexibility due to underlying spasticity. Rigid pelvic obliquity is common and is frequently associated with hip dysplasia or dislocation. ¹² Hyperkyphosis is less prevalent than in low-tone patients, and respiratory decline is generally less pronounced.

Figure 2.

18-year old male patient with low-tone NMS secondary to SMA type II. Preoperative (A) radiographs demonstrate a 100° curve magnitude and 22°, along with hyperkyphosis that is frequently seen in these patients. Traction (B) radiographs show good flexibility, and a T3 to pelvis posterior spinal fusion was performed with multiple posterior column osteotomies. Postoperative (C) radiographs show excellent correction, main curve reduced to 18° and pelvic obliquity was 2°.

Pelvic obliquity is a common and important clinical finding in patients with NMS. This deformity can be classified into three groups based on where the deformity originates: suprapelvic, intrapelvic or infrapelvic. ¹³ Suprapelvic pelvic obliquity is caused by a long scoliotic deformity extending into the pelvis, whereas infrapelvic pelvic obliquity is generally driven by hip contractures. The implications of this classification for treatment remain a subject of debate.

Clinical manifestations of neuromuscular disorders are not limited to spinal deformities; rather, they span a wide range of features, including but not limited to cognitive impairment, hand functions, and head control. Different neuromuscular disorders exhibit significant differences in these features as well, just as they do with spinal deformity. Cognitive impairment is etiology dependent, however high-tone neuromuscular disorders more commonly present with cognitive impairment: 46% of patients with CP had cognitive impairment (intelligence quotient-IQ<70), and the severity and frequency increases with increased neurologic involvement. ¹⁴ Patients with dyskinetic CP may have higher cognitive capabilities when compared with GMFCS matched spastic CP patients. ¹⁵ Low-tone neuromuscular disorders, especially ones characterized with progressive deterioration such as SMA and DMD, cognitive impairment is less frequent and severe. Patients with SMA, especially types II and III preserve normal cognitive function, with only 3% reported to have mild impairment. ¹⁶ Due to the important role played by several dystrophin isoforms in the brain, intellectual disability is a well-known component of DMD, with 22% of patients having an IQ of <70. ¹⁷ There are important nuances across underlying etiologies; however, in general, patients with low-tone NMS tend to demonstrate higher cognitive function and more effective communication abilities.

Hip displacement is another orthopaedic manifestation shared by many neuromuscular disorders. In high-tone disorders, the displacement is caused mainly by muscular imbalance. This is seen in approximately 33% of patients with CP. ¹⁸ Hip deformity also frequently precedes scoliosis. ¹⁹ PO is considered the biomechanical link connecting the hip and the spine. The elevated side of the pelvis generally corresponds to the concavity of the scoliotic curve and is often associated with the more severely displaced hip. ²⁰ Majority of these children with dislocated hips will develop pain and have reduced quality of life, and are likely to require surgery. ¹⁸ In low-tone neuromuscular disorders such as SMA, the underlying mechanism of hip displacement is progressive muscle weakness. With historically higher rates of re-dislocation after surgery and the shorter life span, painless hip dislocations can be monitored in non-ambulatory patients with SMA. Recent evidence, however, suggests that in the era of disease-modifying treatment options (DMTs), these patients are more likely to become candidates for major hip reconstruction surgery. ²¹ Some other neuromuscular disorders, such as DMD, on the other hand, are unlikely to be associated with hip displacement. The timing and sequence of spinal fusion and hip reconstruction also remain topics of considerable debate. A study of 67 patients with CP reported that posterior spinal fusion did not alter the progression of hip displacement, suggesting that spinal fusion may take precedence in the treatment sequence. ²² However, it remains important to recognize that acutely painful hip dislocations may require earlier intervention to improve patient comfort and overall outcomes. Available evidence regarding this issue in low-tone disorders is scarce; therefore, an individualized, case-by-case approach is recommended.

Hand and upper extremity functions also follow significantly different patterns. High-tone patients with spasticity often have contractures, fluctuating tone changes, dystonia, and impaired motor control and coordination. Depending on the severity of neurologic involvement, these features can be extremely disabling: as an example, over 60% of patients with CP were found to have more than minor problems with hand function. ²³ Bimanual performance increases and reaches a maximum between ages 3 to 8, however, depending on the degree of involvement, fine skills are usually severely impaired. ²⁴ Low-tone disorders such as SMA and DMD have progressive decline, and in a proximal-to-distal fashion. This allows fine skills to be relatively preserved early in the disease, to be later diminished severely, especially in DMD in which treatment options are more limited.^25,26 DMD also demonstrates an interesting relationship between hand dominance and scoliosis, with 96% of patients developing a curve with convexity toward the dominant hand side. ²⁷

Etiology

To date, the precise mechanisms driving the development of neuromuscular scoliosis have yet to be fully defined. The manifestation of spinal deformity in both low and high tone neuromuscular conditions suggests a pathophysiological mechanism more complex than isolated muscle weakness or tone, pointing toward a multifactorial etiology. Contributing factors include asymmetric muscle strength and tone, impaired cortical control of the muscle groups, and diminished or absent afferent sensory input, all of which influence the developing spine and predispose it to coronal plane deformity. ²⁸ In the growing population, asymmetric loading may also lead to progressive deformity by growth modulation as attributed to the “Hueter-Volkmann Law”, which, to our knowledge, has not been studied in detail on the neuromuscular population. ²⁹

Epidemiology and Natural History

The large number and complexity of the various underlying conditions makes NMS difficult to generalize, and the available literature on the prevalence and natural history mostly focuses on the more common diagnoses, such as CP and SMA.^19,30,31 It is well established that spinal deformities occur with markedly greater frequency in individuals with neuromuscular conditions than in the broader demographic, and more severe neuromuscular involvement means higher risk for scoliosis, which is a trait shared by both low tone and high tone neuromuscular disorders. Children with mild cerebral palsy, level I on Gross Motor Function Classification Scale (GMFCS), have a risk close to that of the normal population with 2.9%, meanwhile traumatic quadriplegia or high thoracic level paraplegia in skeletally immature patients carries a striking risk of almost 100%.^19,32

Age of onset is variable, ranging from 1 to 20 years. ² However, neuromuscular scoliosis generally appears earlier than adolescent idiopathic scoliosis: average age at onset was reported to be 6.6 years (range 1-20). ³³ Underlying pathology has the potential to significantly alter the natural course of scoliosis. Low-tone disorders such as SMA and DMD typically follow a course of progressive weakness which contributes to deformity progression. For practical treatment decision-making, curves greater than 40° are commonly considered progressive in the literature and are typically viewed as an indication for intervention.

The overall prevalence of scoliosis (Cobb angle ≥10°) in a total population of CP was found as 41%. ²⁸ It is well known that CP constitutes a heterogenous population, and the epidemiology of scoliosis can be better analyzed when stratified according to disease severity. A study on a national database reported that at the age of 20, the cumulative risk of developing severe scoliosis (Cobb angle ≥40°) goes up to 75% in GMFCS V CP. ³⁴ Severe scoliosis was almost exclusively seen in GMFCS IV and V, and children at GMFCS V had a ten-fold higher hazard of developing severe scoliosis compared with those at GMFCS III (hazard ratio-HR:10, 95% confidence interval-CI: 4.5-24, p<0.001). Figure 1 demonstrates a patient with GMFCS V CP, who developed severe scoliosis. With >95% inclusion of the total population with CP in the region, this database provides a strong resource for epidemiological studies. ³⁴

It was reported on patients with GMFCS levels IV and V CP that progression occurred at a rate of 9.7° per year between the ages of 3 and 5. ³⁵ This rate gradually declined to approximately 2–3° per year after the age of 11 until skeletal maturity. Multivariate logistic regression analysis identified the following independent risk factors for the development of severe scoliosis (≥40°): initial Cobb angle, a Cobb angle ≥30° at 10 years of age, and GMFCS level V.

Progression after skeletal maturity plays a key role in treatment decision-making in NMS. It helps identify patients who may require future interventions, determine appropriate follow-up intervals, and guide counseling of caregivers. Despite its clinical relevance, relatively few studies have addressed this topic, likely due to the heterogeneity of this patient population, complexity of their care and the gap in their care while transitioning from childhood to adulthood. In one of the most frequently cited studies in this area, Saito et al. evaluated 37 institutionalized patients with spastic CP with a mean follow-up of 17.3 years. ³⁶ They reported that patients with a Cobb angle ≥40° at age 15 had an 85% likelihood of progressing beyond 60°, whereas the risk was only 13% among those whose curves remained below 40° at that age. A recent systematic review identified two main risk factors for curve progression after skeletal maturity: larger curve magnitude at the end of adolescence (although no universal cutoff was defined, most studies reference thresholds of 40° or 50°) and more severe neurologic impairment (GMFCS levels IV and V). ³⁷ Conversely, curves measuring less than 20° were less likely to progress.

Intrathecal baclofen pumps and selective dorsal rhizotomy were associated with changes in the progression rate of scoliosis, but there is ongoing debate in the literature. Baclofen pumps were associated with increased progression by the earlier series, however, later comparative studies showed no effect. ³⁸

SMA is another neuromuscular disorder burdened by a high risk of scoliosis. Historically, risk of developing scoliosis reached up to 90% in these patients. ³⁹ However, SMA is now a treatable disease and the natural history has significantly improved since the development of DMT options such as the first antisense-oligonucleotide agent, Nusinersen. ⁴⁰ Spinal deformity remains a major problem in this patient population; however, emerging evidence suggests that this new treatment paradigm may reduce the risk of developing scoliosis: a recent study by Ciftci et al. on 165 patients with SMA (51% were treated with DMTs) and an average follow up of 9.8 years reported that DMT was a strong protective factor against developing scoliosis. ⁴¹ Despite this protective effect, scoliosis remains to be a major problem: overall prevalence of clinically relevant scoliosis (Cobb angle ≥40°) was 79%, and when stratified according to disease type, types I, II and III had 90%, 88% and 50% prevalence, respectively. With continued advances in prenatal and perinatal screening leading to early treatment, these prevalence estimates may continue to change in the future.

Most of the literature published on natural history of scoliosis in SMA is on patients with no exposure to DMTs. A study by Wijngaarde et al. on 36 patients with SMA (majority Type 2) reported that mean scoliosis progression was 7.2°/year, which increased to 10.1°/year in the 18 months before surgery, which occurred at a median age of 7.9 years. ⁴² A patient with type 2 SMA and severe scoliosis can be seen on Figure 2. A recent study comparing 46 untreated patients with 39 patients receiving DMTs suggested that, when initiated sufficiently early, these therapies may slow curve progression and prevent the deformity from reaching a 50° threshold. ⁴³ For optimal benefit, treatment should begin before the Cobb angle reaches 26° or before 4.5 years of age. In that setting, the mean rate of progression decreased from 10.1° per year to 5.6° per year. It is important to recognize that these therapies are likely to shift the patient population by bringing into consideration individuals who were previously deemed too medically fragile for intervention, such as SMA type 1, through improvements in cardiac and respiratory function and extension of life expectancy. ¹⁰ The success of DMT is highly dependent on the timing of treatment initiation, and wider, more standardized adoption of these agents may significantly alter the clinical manifestations of SMA in the future.

Another low-tone neuromuscular disorder, DMD, is also burdened by a high risk of developing scoliosis. It was reported that the prevalence of having NMS reaches up to 72% by 20 years of age. ⁴⁴ The onset and timing of scoliosis in these patients typically correlates with the loss of ambulation and most commonly occurs during the second decade of life, in contrast to another low-tone disorder, SMA. A recent study reported the median age of scoliosis onset to be 12 years (interquartile range, 11–15). ⁴⁵ Following the loss of ambulation, when patients spend the majority of their time in a seated position, scoliosis progresses at an average rate of 6°/year. ⁴⁶ Notably, the rate of progression after loss of ambulation appears to be independent of age. Corticosteroid treatment has significantly improved outcomes in DMD by delaying the loss of motor milestones and decreasing mortality risk. ⁴⁷ A study on 54 patients with DMD reported that glucocorticoid treatment reduced the risk of developing scoliosis and undergoing surgery from 92% to 20%. ⁴⁸ The recombinant adeno-associated virus vector–based gene therapy Delandistrogene moxeparvovec, recently approved by the Food and Drug Administration (FDA), represents a novel and promising therapeutic strategy that may significantly alter the treatment landscape of DMD. ⁴⁹ However, there is no direct clinical evidence on how gene therapy might affect the development and progression of scoliosis in these patients.

High-tone disorders can benefit from treatments aimed at reducing spasticity and muscle tone; however, their effects on scoliosis progression remain debated. Although earlier reports suggested that intrathecal baclofen pump implantation may accelerate scoliosis progression, subsequent studies have not consistently reproduced these findings and have generally reported no significant effect on curve progression, as demonstrated by Senaran et al.^38,50 Selective dorsal rhizotomy is another intervention that has no clear demonstrated effect on scoliosis progression. ⁵¹

Rett syndrome is another disorder that is associated with a high prevalence of scoliosis. It is a neurodevelopmental disorder seen in female patients and is characterized by an early normal development followed by progressive deterioration of the acquired developmental skills usually starting at the age of 1–2 years. The clinical manifestations change with each stage of the disease: early regression usually comes with hypotonia and weakness, however, as the disease progresses, hypertonia and spasticity become the predominant features. ⁵ In a study on 394 girls with Rett syndrome, Downs et al. reported a mean age of scoliosis onset of 11 years. ⁵² More importantly, patients with a p.Arg255* mutation or large deletion were noted to have significantly earlier onset when compared with the whole cohort (4 years 6 months and 7 years 10 months, respectively). Together with the deformity magnitude and ambulatory status, genetic profile can be used to predict curve progression in these patients.

Medical Comorbidities

In many cases, neuromuscular scoliosis is associated with multiple comorbidities that increase the complexity of surgical care. For instance, cerebral palsy is defined by motor impairments, but 95% of the time it is accompanied by other comorbidities and conditions that can be as disabling as the physical impairments. ⁵³ Severe scoliosis leads to crowding in the thoracic and abdominal cavities, in turn causing decline in pulmonary functions. It is well established that neuromuscular conditions negatively affect respiratory functions, with or without scoliosis. ⁶ A study on 39 patients with neuromuscular disorders and 24 age and sex matched controls reported that the study group had significantly declined respiratory functions compared with the healthy controls. ⁵⁴ It has also been reported that patients who develop NMS exhibit further declines in respiratory function compared with patients with neuromuscular disorders without scoliosis.

As highlighted throughout this review, neuromuscular conditions exhibit substantial heterogeneity, which is also reflected in their respiratory manifestations. Low-tone conditions usually have more profound baseline respiratory muscle weakness and are more vulnerable to respiratory failure. ¹¹ Broadly, SMA leads to more pronounced weakness of the intercostal muscles with relative preservation of diaphragmatic function, whereas DMD is characterized by greater diaphragmatic involvement with comparatively preserved intercostal muscle strength. ¹¹ The natural course of lung functions in SMA is characterized by a progressive decline during childhood and stabilization when adulthood is reached. ⁵⁵ DMTs provided significant benefits on pulmonary functions in these patients, however, respiratory decline remains to be a major issue.^56,57 Although surgical treatment of scoliosis does not appear to result in immediate improvement in respiratory function, it may still be beneficial by preventing or mitigating further decline. ⁵⁸ The available evidence on this matter remains inconclusive.

Cardiac and respiratory failure are the two most common causes of mortality and morbidity in DMD, and with the improvements in medical management, implementation of multidisciplinary care and use of glucocorticoids, mean survival has increased to late twenties. ⁵⁹ Although the evidence remains inconclusive, surgical treatment may slow the decline in respiratory function in these patients. In a study of 199 patients with a mean age of 15 years (average follow-up of 6 years), forced vital capacity (FVC) increased during the first two years after surgery; thereafter, the rate of decline was significantly lower than in the non-surgically treated group (2.8% vs 4.8% per year). ⁶⁰ Similar improvement was also reported for mortality, which was 22% in the non-surgical group during the follow-up (mean 6.4 years) while surgery reduced this to 8.1%. ⁶⁰ These reports should be approached with caution, especially regarding the immediate increase in FVC, since other studies suggest the opposite. ⁶¹

While pulmonary insufficiency is generally more pronounced in low-tone disorders, patients with high-tone disorders also experience substantial respiratory morbidity. A recent study on patients with cerebral palsy and scoliosis who were not treated surgically (mean follow-up 17.8 years) reported that 76.3% of deaths were due to respiratory causes. ⁶² It has long been debated whether surgical treatment improves respiratory function in CP. ⁶³ A newly published study by Ahonen et al. reported that in patients with CP, surgical treatment of scoliosis significantly reduces the cumulative incidence of pneumonia (from 175.5 to 121.5 hospitalizations per 1,000 years, p<0.001). ⁶⁴ More importantly, surgery was found to reduce pneumonia-related mortality (8.9% in patients who were not surgically treated vs 3.3% in patients who had surgery, p=0.008). Considering the large sample size, nation-wide inclusion and long follow-up, this recent study is important because it highlights the broader benefits of surgery in NMS beyond mere deformity correction.

The pattern of cardiac dysfunction can differ markedly depending on the underlying diagnosis. These patterns can be grouped into three as underlined by a recent Scoliosis Research Society (SRS) proceedings report: abnormalities of conduction, function or rhythm. ⁶⁵ Low-tone neuromuscular disorders tend to be associated with more pronounced cardiac morbidity. One important example is DMD: with the use of assisted ventilation to manage respiratory failure in DMD, cardiac dysfunction became the leading cause of death. ⁶⁶ Direct myocardial involvement is mainly a feature of muscular dystrophies. Whether scoliosis surgery affects cardiac function in patients with low-tone neuromuscular disorders remains unknown.

Gastrointestinal disorders are common in children with neuromuscular disorders, which can lead to malnutrition. Malnutrition can be diagnosed with an albumin <3.5 g/L, prealbumin <20 mg/dL and a low body mass index (BMI) (less than 5^th percentile). ⁶⁷ Depending on the underlying neuromuscular condition, presentation of malnutrition can be different: patients with CP are likely to be underweight while over 50% of patients with DMD were reported to be overweight, mostly attributed to the use of glucocorticoids. ⁶⁸

Preoperative Optimization

Preoperative optimization should primarily involve a comprehensive evaluation of the patient’s overall medical status, with the understanding that these neuromuscular disorders extend beyond musculoskeletal manifestations. Many institutions have formed multidisciplinary complex care teams and implemented pathways for these children. ⁶⁹

Patients with day- or night-time hypoventilation, ineffective cough and vital capacity <60% of predicted are at increased risk for respiratory complications in the postoperative period. ⁷⁰ Preoperative respiratory therapy, training for airway clearance techniques and the use of noninvasive ventilation devices may be useful. According to the American College of Chest Physicians guidelines for patients with DMD, preoperative FVC <50% predicted is a marker of increased risk and FVC <30% predicted is considered high risk, and it is strongly recommend that these patients should be extubated directly to non-invasive positive pressure ventilation (NPPV). ⁷¹ Patients with insufficient airway clearance, which is assessed by measuring peak cough flow and maximum expiratory pressure, can be good candidates for preoperative training and postoperative use of mechanical insufflation-exsufflation (MI-E) devices.

Malnutrition must be appropriately treated before the surgery, which may require placement of a gastrostomy tube (G-tube, GJ-tube) for more effective feeding. Gastrostomy tube placement is indicated in patients with malnutrition refractory to oral nutritional interventions, moderate to severe dysphagia, or inability to sustain adequate hydration. It is important to recognize that preoperative optimization must be comprehensive: comorbid conditions such as respiratory failure can adversely affect nutritional status, and interventions like NPPV may, in turn, lead to meaningful improvements in nutrition.

Cardiac dysfunction is a common feature of muscular dystrophies and myopathic disorders, such as DMD. Cardiac evaluation must be done close to the surgery, ideally within 3 to 6 months to have baseline cardiac function information to the treatment team.^66,70 Electrocardiogram (ECG) to establish baseline cardiac function, and an echocardiogram or cardiac MRI (typically over age 6-7 to be able to perform without anesthesia) are recommended to screen for underlying structural abnormalities and also cardiac function.

Radiological Evaluation

A good clinical evaluation is the key for successful treatment of a patient with NMS. A comprehensive assessment should extend beyond radiographic parameters and curve magnitude, incorporating evaluation of curve behavior, functional capacity, and associated musculoskeletal or medical comorbidities.

Flexibility of the spinal deformity is one of the important differences between low-tone and high-tone neuromuscular disorders. Curve flexibility was studied on 107 patients from different etiologies, and in the subgroup of 43 patients with NMS, mean flexibility was found as 38%. ⁷² But low-tone NMS is generally more flexible especially in younger patients, due to the reduced muscle tone and truncal weakness. At the time of initial diagnosis of NMS, patients with Duchenne muscular dystrophy demonstrated a mean flexibility of 76%, which declined progressively to 36% over time. ⁷³ Muscle tone is not the sole determinant of flexibility; increasing curve magnitude and other factors likely contribute to the gradual transition toward a more structural deformity. On the other hand, patients with high-tone NMS typically exhibit spasticity, passive muscle stiffness and contractures, which all play a role in reduced flexibility of the spine. Changes in flexibility with age has not been studied in this population, however, an analysis on 25 patients with CP reported a flexibility of only 25% between preoperative sitting and supine radiographs. ⁷⁴

Indications for advanced imaging in NMS remain ill-defined, with a significant gap in the literature. Magnetic resonance imaging (MRI) is common in early-onset patients, and among a large cohort of EOS, it was reported that 42% of the patients with neuromuscular EOS had a pretreatment MRI. ⁷⁵ The prevalence of abnormal findings was as high as 39%, markedly higher than in other etiologies; however, the impact of these findings on clinical decision-making remains unclear. Most common abnormal findings were Chiari malformation, spina bifida, syrinx and tethered cord. The decision to obtain an MRI must be weighed against the necessity of sedation or anesthesia in many of these patients. Unlike children with CP, SMA and DMD, in whom intraspinal abnormalities are uncommon, children with MMC demonstrate a very high rate and the utility of advanced imaging is potentially higher. Tethered cord was found in 89% of the patients while 76% had Chiari malformation and 11% had syringomyelia. ⁷⁶ Computed tomography (CT) is another advanced imaging modality that can be used in select cases, especially for surgical planning. Complex deformities are more effectively visualized on CT imaging, which, with the increasing use of computer-assisted navigation systems, can also facilitate accurate instrumentation. ⁷⁷ Complex deformities which require extensive preoperative planning may also benefit from patient-specific models based on 3D CT reconstructions.

Non-Operative Management

Non-operative management of scoliosis has limited effectiveness in NMS. ⁷⁸ In most cases, non-operative management is an interim measure while waiting for surgery. The impact on curve severity may be limited, however conservative management can still have functional benefits: maintaining stable sitting position, facilitating upper limb use, preventing abdominal compression from trunk collapse and improving diaphragm excursion.

Despite achieving an initial correction, bracing does not appear to provide sustained deformity control in the long term and is generally ineffective in preventing progression. In a cohort of 86 patients with spastic quadriplegic CP, treatment with a thoraco-lumbo-sacral orthosis (TLSO) resulted in an initial correction of 37%, with the mean Cobb angle improving from 68° to 43°. ⁷⁹ The curve progression was also reported, with average of 4.2° per year. More recently, attention is turned from hard shell TLSO braces to other types that offer a more comfortable wear. A dynamic spinal brace has shown similar results to TLSO, with an initial correction of 34.3% reducing to 19.3% during follow-up. ⁸⁰ More importantly, the rate of brace intolerance was only 3.5%. A recent systematic review on the effectiveness of bracing in children with CP confirmed the limited success of this treatment modality. ⁷⁸ Other non-operative treatment modalities in patients with high-tone NMS are medical management of hypertonia, optimized seating systems and physical therapy. Although these interventions may not directly affect deformity progression, they improve overall function and quality of life. Furthermore, bracing may be used to delay surgical intervention, allowing additional spinal growth and potentially facilitating a more favorable timing for surgery.

The evidence of brace use in patients with low-tone NMS is even more limited in the literature. A recent trial suggested a potential beneficial effect of TLSO use on scoliosis in patients with SMA; however, the magnitude of this effect was quite small, and in the absence of supportive future evidence, these findings should be interpreted with caution. ⁸¹ Most importantly, in the presence of severe muscular weakness and hypotonia, bracing should be used cautiously, as it may compromise pulmonary function and contribute to chest wall deformity.

Operative Management

Indications for operative treatment in patients with NMS can vary widely based on the underlying disorder and the patient’s medical condition. Patients with neuromuscular scoliosis, as highlighted in the preceding sections, commonly present with multiple medical comorbidities and highly complex care needs. Multidisciplinary approach prior to surgery is mandatory to ensure good outcomes. As surgical techniques continue to evolve and non-orthopedic medical care advances, surgical treatment can now be applied safely in most patients.

The main principles of surgical treatment of NMS are similar across different diagnoses: stabilize the spine and prevent progression, achieve sitting balance in non-ambulatory patients, improve quality of life for both patients and caregivers. Pain resulting from costopelvic impingement may also constitute an indication for surgical intervention and is typically observed in patients with large curves. Detailed surgical strategies are tailored based on the underlying diagnosis. In CP, the decision to include the pelvis into the fusion mostly involves ambulatory status as one of the main determinants. A study on 87 patients from prospective databases attempted to establish the risk factors for failure when fusion is stopped at L4 or L5 ⁸² : pelvic obliquity of ≥17° and dependent sitting status as preoperative characteristics were associated with unsatisfactory correction if the fusion was stopped at L4 or L5. The risk of decompensation was 72% when both factors were present. In low-tone NMS, terminating the fusion at L4 or L5 is appropriate only in a small, carefully selected subgroup of patients, and is generally less favored than in high-tone NMS. The main reason for this is the risk of progression of the underlying disease. Ambulatory patients with proximal muscle weakness may be suitable candidates for fusion short of the pelvis in an effort to preserve ambulatory capacity. However, if the patient becomes wheelchair-dependent during follow-up, extension of the fusion to the pelvis should be strongly considered.

Despite the success and durability of posterior spinal fusion, early-onset scoliosis in this population still presents a major challenge. Principles of treatment may be similar for both low-tone and high-tone patients, but characteristics of the underlying disease can affect surgical technique or the implants used. Parasol deformity, which occurs specifically in low-tone patients, may require special adjustments to growth-friendly treatment. Both magnetically controlled growing rods (MCGR) and traditional growing rods (TGR) can be expected to play a role in the treatment (Figure 3). Adding lateral chest wall support to growth friendly constructs to address the collapsing parasol rib deformity has been demonstrated to increase chest wall width, which may in turn improve pulmonary functions. ⁸³ Vertical expandable prosthetic titanium rib (VEPTR) is another method that was introduced to prevent thoracic insufficiency syndrome and address parasol deformity in low-tone patients. Popularity of this method has significantly reduced over time, but it can still be an option in select patients with chest wall deformity.^7,84 Hyperkyphosis is a relative contraindication to MCGR use. ⁸⁵ As previously underlined, low-tone neuromuscular disorders are more likely to exhibit increased kyphosis, which is most pronounced in SMA. ¹⁰ TGRs may be a more appropriate choice in this setting. Another important consideration is curve flexibility: it has been argued that the distractive force generated by MCGRs may not be adequate to overcome a stiff curve. ⁸⁵ High-tone NMS, characterized by spasticity, may represent a favorable indication for TGRs. The Shilla system represents another useful option for early-onset NMS, particularly in medically complex patients, as it may decrease the cumulative surgical burden during treatment period. Results have not been extensively analyzed on NMS, and available literature places it as an acceptable alternative to MCGRs, with comparable outcomes but with significantly less surgical procedures. ⁸⁶

Figure 3.

Early-onset scoliosis in the setting of cerebral palsy, with 84° curve magnitude and 12° PO (A). Growth-friendly surgery was performed at the age of 9, by using MCGRs, achieving 50% correction in the main curvature, and a level pelvis after the index surgery (B). No complication occurred during the lengthening period, and definitive fusion was planned when the patient reached Sanders maturity scale of 7, at the age of 13. The broken rod (C) was noticed right before the definitive fusion, and this was treated as part of the fusion procedure, thereby not requiring an unplanned return to the operating room. Before definitive fusion (C), curve magnitude is 77°, which decreased to 46° after posterior spinal fusion (D). PO remained at zero.

Surgeons are increasingly favoring delaying the surgery in neuromuscular EOS when possible. This is most certainly due to the higher risk of complications associated with younger age at initiation. ⁸⁷ Another important message is delivered by a recent SRS consensus report: while younger children are more likely to be treated with growing rods, at the age of 9, fusion is preferred. ⁸⁸ This reflects the success of spinal fusion, as it would likely only be a single procedure rather than undergoing multiple surgeries with a growing rod construct. Early spinal fusion carries the risk of the crankshaft phenomenon; however, this complication has not been extensively studied in neuromuscular patients, and the available literature suggests a relatively low incidence in this population.^89,90

Once neuromuscular scoliosis reaches approximately 40°, it is generally considered progressive, and surgical intervention is typically considered when the deformity begins to negatively impact the patient’s quality of life. Delaying the surgery was reported to negatively impact the outcomes: a recent study showed that curves ≥80° have greater residual curve magnitude after surgery, as well as an increased risk of certain complications (neuromonitoring signal changes, odds ratio: 3.07, p=0.003), requirement for utilizing adjunct surgical techniques, increased blood loss and surgical time. ⁹¹ Despite these suggested advantages of early surgical intervention, the decision-making process is complicated and is not driven by Cobb angle alone.

When spinal fusion is indicated, pedicle screw-based constructs, combined with strong pelvic fixation especially in the non-ambulatory patients, are widely preferred, and provide effective correction of the curve. S2-alar-iliac (S2AI) screws have demonstrated lower complication and revision rates compared with traditional iliac screws, and have consequently emerged as a preferred method of pelvic fixation—particularly in patients at increased risk for skin and wound complications.^92,93 Further studies are required to clarify if this advantage extends to radiographic outcomes as well. As an alternative to spinal fusion, a minimally invasive fusionless method was also recently proposed. ⁹⁴ This 5-year follow-up study reported 61% curve correction (mean 35° at final follow-up) and a 7.2° final pelvic obliquity, with a complication rate of 31.3%. This system offers a self-expanding mechanism that allows longitudinal growth. A similar system (one-way self-expanding rod, OWSER) has also been proposed for early-onset NMS, and results were reported for a slightly younger group of patients, with a mean age of 9.6 years. ⁹⁵ T1-S1 height increased by a mean of 1 cm during the 2 year follow-up period, and the mean scoliosis angle improved from 80° to 39° (Figure 4).

Figure 4.

A 15-year old female patient with GMFCS V spastic CP can be seen in figures A to C. (A) C-shaped left convex neuromuscular scoliosis. 3 months (B) and 2-year (C) follow-up after definitive bipolar posterior instrumentation with a double rod construct. A 6-year old female patient with GMFCS V spastic CP is seen in figure D to H. C-shaped right convex neuromuscular early onset scoliosis (D). 3-month (E), 6-month (F), 1-year (G) and 2-year (H) follow-up radiographs after bipolar posterior instrumentation with a one-way self-expanding rod (OWSER) system.

Osteotomies may also be indicated for large, rigid curves with severe PO (Figure 5). Bekmez et al. proposed an algorithm based on PO correction observed on traction radiographs under general anesthesia. When PO measured ≥15° on traction imaging, a pedicle subtraction osteotomy (PSO) achieved significantly greater correction when compared with multiple posterior column osteotomies (84% vs 59%, p = 0.001). ⁹⁶ While osteotomies offer superior deformity correction, their use must be balanced against the increased risks associated with longer operative time and greater blood loss.

Figure 5.

14-year old female patient with SMA type II and low-tone NMS. Curve magnitude is 142° on preoperative (A) radiographs, along with a severe PO measuring 34° and hyperkyphosis. Flexibility was limited as demonstrated by radiographs under traction (B), and a decision was made to do a vertebral column resection at T10. Good coronal balance and excellent correction of pelvic obliquity was achieved postoperatively (C).

Historically, postoperative management of these patients involved prolonged intensive care unit (ICU) stays. Recent evidence has shown that this decision must be made on a case-by-case basis, and ICU stay can be avoided in many of these patients. On patients with GMFCS IV and V CP, Shaw et al. reported that with the implementation of an enhanced recovery after surgery (ERAS) protocol, the rate of ICU admission was as low as 38.8%. ⁹⁷ Brooks et al. revealed that the primary predictor of the length of ICU stay was the institution where the surgery was performed. ⁹⁸ It was suggested that postoperative ICU disposition should not be based on institutional traditions, and a patient and case-based assessment may help allow regular unit dispositions, especially in patients with <4 hour surgical time.

Surgical decision-making in these patients is further complicated by ethical controversies regarding children with severe cognitive impairment. As previously mentioned, high-tone disorders are more frequently associated with severe cognitive impairment, and their surgical treatment should be guided by the fundamental principles of non-maleficence and beneficence. ²⁴ Meanwhile, most low-tone disorders do not cause severe cognitive impairment and therefore patients can be involved in surgical decision-making according to their age and maturity (“assent”). Another controversy is with resource utilization: traditional cost-effectiveness frameworks may place patients with rare, life-limiting neuromuscular disorders in a position of disadvantage, whereas public funding for these high-cost therapies raises legitimate concerns regarding distributive justice. While these ethical questions are out of the scope of this article, current professional society perspectives emphasize the importance of avoiding disability-based discrimination. ⁹⁹

Another important consideration in the operative treatment of these patients, is the management of special anesthetic concerns. One such example is DMD: total intravenous anesthesia (TIVA) should be used for induction and maintenance, and succinylcholine strictly contraindicated due to the risk of severe fatal rhabdomyolysis, hyperkalemia and cardiac arrest. ⁶⁶ This example underscores the importance of management by a multidisciplinary team with expertise in the treatment of a broad spectrum of neuromuscular conditions.

Complications

With advances in surgical techniques, perioperative care, and a better understanding of the underlying pathologies, surgical treatment of neuromuscular scoliosis can be performed with improved safety. A large database study revealed a 10% reduction in the complication rates between 2004 to 2015. ¹⁰⁰ When evaluating trends, it is also important to recognize that with recent advances, increasingly complex patients have become candidates for surgery; for example, children with SMA type 1, who were previously considered medically unfit for spinal surgery, can now be treated surgically. ¹⁰

When compared with idiopathic scoliosis, surgical treatment of NMS is associated with a higher incidence of perioperative and postoperative complications. A recent meta-analysis analyzing the last 10 years, which captures the pedicle screw era, showed an overall complication rate of 38% in 2155 patients. ¹⁰¹ Wound related complications were the most frequent, with a pooled rate of 13.3%. This was followed by respiratory (11.8%), implant related/mechanical (7.1%), gastrointestinal (5.2%), pseudoarthrosis (4.7%) and neurologic complications (2.9%). 9.6% of the patients required revision surgery, and 56% of the revisions were due to wound related complications. Mortality rate was 0.9%.

In line with our prior discussion on low-tone NMS, respiratory complications demonstrated a significant correlation with DMD and SMA. ¹⁰¹ Duckworth et al. reported that patients with DMD had a complication rate of 38.5%, which was significantly higher than other neuromuscular conditions (16.7%, p=0.019). ¹⁰² DMD also warrants special attention for cardiac complications because of the high frequency of underlying cardiac dysfunction, and monitoring for hepatotoxicity which was reported only in this population. ¹⁰² However, low muscle tone is not the only determinant of respiratory complications, as patients with Rett syndrome were also pointed out as a high risk population, with a significantly higher risk of postoperative respiratory failure when compared with CP (43% vs 19%, p=0.02). ¹⁰³

Patients in this high-risk group of low-tone NMS may warrant modified management strategies, an issue addressed by Ozhan et al.: a two-surgeon approach was used in 16 patients with low-tone neuromuscular disorders, which reduced ICU admissions from 100% to 23%, and length of stay (LOS) from 5.9 to 4.7 days. ³ This approach also significantly reduced operative time, intraoperative blood loss and transfusion requirement. Multidisciplinary collaboration with standardized clinical care pathways were also reported to successfully decrease LOS by multiple studies.^104,105 Operative treatment constitutes only one facet of care in this population; optimization of perioperative and non-surgical factors is also very critical for improving outcomes and ensuring safety.

Outcomes

With modern techniques and improvements in patient care, surgical treatment for NMS significantly increases the health-related quality of life (HRQOL) and ease of care. A study on 69 patients with CP showed that after surgery for scoliosis, the “Caregiver Priorities and Child Health Index of Life with Disabilities (CPCHILD)” questionnaire scores improved by a mean of 7.19 points at 1 year, which was maintained at 2 and 5 years. ¹⁰⁶ Despite a substantial 1-year complication rate of 46%, these findings suggest that surgical treatment of NMS confers significant value in terms of improvements in HRQOL and caregiver satisfaction. These improvements are most likely the result of improved positioning, personal care, comfort and pain. In certain subgroups such as ambulatory patients, outcomes are approaching that of idiopathic scoliosis. ¹⁰⁷ Another striking example is reported by Jain et al.: on 212 patients with CP, 74% of caregivers reported that the overall quality of the patient’s life was a lot better, and 16% reported that it was at least a little better. ¹⁰⁸ They rated spinal surgery as more beneficial than other common orthopaedic interventions, second only to G-tube placement in perceived overall benefit.

Objective outcome assessment in this population is limited by challenges in effective communication and the broad heterogeneity of the patient group. It should be acknowledged that the evaluation of outcomes in this cohort is further limited by the lack of specific and validated assessment tools. CPCHILD and CP QOL-Child and Teen are validated tools for use in children with CP. ¹⁰⁹ However, lack of specific tools for other neuromuscular disorders is a concern and must be a topic for future research.

Another important outcome of surgical treatment for NMS is in the mortality rates. Whether surgical intervention alters the risk of pulmonary complications and mortality has been a longstanding matter of debate. ¹¹⁰ As we discussed above, emerging evidence by Ahonen et al. suggests that in patients with CP, surgery reduces pneumonia-related mortality (8.9% in patients who were not surgically treated vs 3.3% in patients who had surgery, p=0.008). ⁶⁴ The debate persists for other neuromuscular disorders, particularly low-tone, given their greater susceptibility to respiratory decline. Similar outcomes have also been reported for DMD: Yang et al. reported on 199 patients with a mean follow-up of 6.4 years and reported a lower mortality rate in the surgically treated group (22.0% in the non-surgical group vs 8.1% in the surgical group, p<.001). ⁶⁰ As previously mentioned, this improvement was accompanied by an increase in FVC for 2 years following surgery, and a decline at a slower rate afterwards.

Conclusion

Neuromuscular disorders represent a diverse and complex group of conditions, each with unique clinical features, and that muscle tone is only one of several factors contributing to orthopaedic manifestations. Despite these limitations, this framework offers important advantages over existing classification systems by improving the understanding and characterization of neuromuscular spinal deformities.

In summary, distinguishing low-from high-tone neuromuscular spinal deformities provides a clinically meaningful framework that extends beyond traditional etiologic classifications, offering important insights into deformity characteristics, progression patterns, comorbidity profiles, and treatment strategies. Similar surgical principles are applied to both groups; however, important nuances exist in other aspects of management. Table 1 summarizes the key differences detailed in the text. Both groups carry a substantial burden of comorbidities and require complex care; however, with thorough preoperative optimization and good surgical decision-making, spinal surgery can be performed safely, and provide very meaningful improvements in the quality of life for both patients and caregivers.

Table 1.

Summary of the key differences of low-vs high-tone NMS.

​	High-tone	Low-tone
Clinical presentation	Characterized by spasticity, rigidity, and reduced flexibility. Curves are often stiff, with associated pelvic obliquity and frequent hip subluxation/dislocation. Cognitive impairment and impaired hand function are more common.	Marked by hypotonia and truncal weakness, leading to more flexible, long C-shaped curves often with significant kyphosis. Respiratory compromise is more prominent, and cognitive function is generally better preserved.
Natural history	Early onset with rapid progression in severe cases, particularly in non-ambulatory patients. Progression may continue after skeletal maturity, especially with larger curves.	Progressive deformity driven by ongoing muscle weakness, often accelerating after loss of ambulation (e.g., DMD). Emerging therapies may slow progression if initiated early enough, as in SMA.
Medical comorbidities	Frequently associated with cognitive impairment, seizures, and other orthopedic issues such as hip instability. Respiratory dysfunction is present but typically less severe than in low-tone disorders.	Significant respiratory muscle weakness and higher risk of pulmonary failure. Cardiac involvement is common in muscular dystrophies, along with nutritional challenges.
Preoperative optimization	Focus on managing spasticity, nutritional status, and respiratory condition. Multidisciplinary care is essential, and postop ICU stay can be avoided with good preoperative optimization.	Emphasis on respiratory optimization (e.g., NPPV, airway clearance), cardiac evaluation (especially in DMD), and aggressive nutritional support, often including gastrostomy.
Radiologic evaluation	Typically demonstrates stiff, less flexible curves with lower correction on bending or supine films. Advanced imaging may be used selectively.	Greater initial flexibility, especially early in disease, with progressive stiffening over time. Imaging may also reveal associated kyphosis and thoracic deformities.
Non-operative management	Limited impact on curve progression; includes bracing, tone management, seating adaptations, and physical therapy for functional support. Can be used to temporize surgery until skeletal maturity.	Even more limited role for bracing, with caution due to potential respiratory compromise. Focus is on maintaining function and delaying surgery when possible.
Operative management	Often requires fusion to the pelvis, especially in non-ambulatory patients with pelvic obliquity. Select cases may be effectively treated with fusion short of pelvis.	Surgical strategy may only allow shorter fusion in select cases, less frequent than high-tone NMS due to the risk of progression of the underlying disease.
Complications	Overall high complication rates, including high wound and implant-related issues. Spasticity, medical comorbidities, malnutrition and poor soft tissue quality contribute to risk.	Higher rates of respiratory and cardiac complications, particularly in SMA and DMD. Longer postoperative ICU stays. May benefit more from a two-surgeon approach.
Outcomes	Improvements in quality of life, sitting balance, and caregiver burden are well documented. Evidence on positive impact on pulmonary function, and reduced mortality after surgery is emerging.	Functional and quality-of-life improvements are seen, though outcomes are influenced by underlying disease progression. Recent evidence suggests that surgery benefits in slowing respiratory decline and reducing mortality in DMD. SMA mostly benefits from disease-modifying treatment options.

ORCID iDs

Riza M. Cetik https://orcid.org/0000-0001-9390-4129

Muharrem Yazici https://orcid.org/0000-0003-1532-7260

Ethical considerations

Ethical board approval is not required for this review article.

Data Availability Statement

Data collected and used for this study can only be provided upon reasonable request from the corresponding author. Data sharing is at the authors’ discretion.*