Musculoskeletal changes and treatments in paediatric spinal cord disorders: A scoping review

Abstract

Purpose:

This study aimed to highlight the structural and functional musculoskeletal changes and associated treatment strategies in paediatric patients with spinal cord disorders (SCD).

Methods:

A systematic scoping review was conducted whereby PubMed, Excerpta Medica Database and MEDLINE Ovid databases, and grey literature were searched for articles published between January 2000 and June 2024. Study criteria included at least 50% of participant cohort being children aged under 18 years at time of SCD diagnosis, investigating the musculoskeletal effects of SCD in children, and related management or interventional strategies. Reports in which paediatric or SCD participants were less than 50% of the cohort were included if results were appropriately stratified. Included reports underwent descriptive analysis.

Results:

Forty-five reports were eligible for inclusion. Physiological Parameters, Musculoskeletal Complications, and Interventions were the main themes identified. It was observed that musculoskeletal changes following SCD can differ in children compared to their adult-injured counterparts, but the mechanisms underlying these differences are not known. Intervention studies that have been performed are important, but underpowered, and cannot yet be translated into routine care.

Conclusion:

Monitoring and treatment guidelines for musculoskeletal health in this population are scarce. Comprehensive research efforts are required to facilitate guideline development, which will be imperative in improving musculoskeletal outcomes following paediatric SCD.

Keywords

paediatrics spinal cord injuries spinal cord diseases bone and bones musculoskeletal system

Introduction

Paediatric spinal cord disorders (SCD) are rare, but the impact of SCD in childhood is significant. However, perhaps due to the rarity of this population, studies investigating the effects of SCD on the musculoskeletal system in children are lacking. The term SCD includes both traumatic spinal cord injuries (SCI) and non-traumatic spinal cord dysfunction aetiologies, of which 3.8 and 6.5 per million children younger than 15 years are diagnosed per year in Victoria, Australia, respectively.¹ This aligns with the global incidence of traumatic SCI in children, with 4.3 per million children per year under 15 in developed countries,² and between 3.3 to 13.2 per million throughout global regions.³

Following a SCD, abnormal sensory and motor function below the level of injury results in the loss of the typical load on the bones from weight-bearing and muscle activity. As a result, there is a change in bone structure and disruption of bone growth below the injury site.^4–6 The musculoskeletal system is still developing in children, so the effects of SCD on their bones can vary from the effects seen in adults who suffer injury to the spinal cord.⁷ Bone mineral density (BMD), as measured using dual X-ray absorptiometry (DXA) and peripheral quantitative computed tomography (pQCT), is heavily reduced in both children and adults with SCD.^8,9 In addition, children have an increased risk of developing musculoskeletal complications such as scoliosis, hip dysplasia, and fractures.^10–12 Scoliosis and hip dysplasia are the two most common orthopaedic complications that arise following a SCD.^13,14 Fracture risk is high in paediatric-onset SCD, as these patients live with this condition for the majority of their lifespan. Their compromised bone health, combined with significant injury duration, often results in fragility fractures which contribute to increased pain and reduced quality of life.¹³ Furthermore, children with SCD may never attain peak bone mass levels. Peak bone mass is determined by nutritional, endocrine, and environmental factors such as physical activity,¹⁵ which can be heavily disrupted following a SCD diagnosis. Despite these differences, paediatric SCD literature is scarce. The statistics surrounding paediatric SCD are not as well documented as for their adult counterparts, and there is currently no standard reporting procedure or data registry that exists for the paediatric SCD population in Australia.

A recent systematic review of the literature revealed that between 1974 and 2020, 176 reports were published that concerned paediatric SCD, of which only 36 looked at neuromusculoskeletal and movement-related structure and function.¹⁶ Therefore, many aspects of care for this population may not be receiving adequate attention. While rehabilitation research and clinical practice guidelines (CPGs) are established in adult SCD, there are still substantial gaps in literature,^17,18 which is even more evident in the paediatric SCD population.^19,20 CPGs for the management of musculoskeletal complications that arise from SCD in children are needed. The International Perspectives on Spinal Cord Injury report provides excellent recommendations for persons living with an SCI;²¹ however, these recommendations are not specific to children, and the concepts are not explored in original paediatric research elsewhere. Developing CPGs to support musculoskeletal outcomes will be key to improving quality of life and reducing the risk of pathological fracture and bone deformities that are often associated with paediatric SCD, given that these patients will live with the consequences of their injury for their lifetime.

The aim of this review was to broadly map the musculoskeletal changes following SCD in children. Therefore a scoping rather than systematic methodology was used.^22–24 A scoping review of the available evidence was performed because, unlike systematic reviews, scoping reviews attempt to provide an overview of a research topic and can include evidence from a variety of sources.^22,23 Systematic reviews typically provide evidence regarding the effectiveness of interventions. Thus the specificity of the research question means they are of limited scope.²⁴ Conversely, scoping reviews provide the opportunity to review many factors that contribute to a research question, while being produced in a systematic manner. Therefore, a scoping methodology was adopted for this review. This review was conducted according to the methodology outlined by Arksey and O’Malley²² and refined by Peters et al.²⁴ The purpose of this scoping review was to explore how SCD diagnoses have been shown to impact the musculoskeletal system of children in the current literature. Therefore, the question driving the basis of this scoping review was: “What are the structural and functional musculoskeletal changes and associated treatment strategies in paediatric patients with spinal cord disorders?”

Methods

Methodology and reporting

This review is reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA-ScR)²³ guideline. The protocol for this review was pre-registered on the Open Science Framework (OSF) Registry, registration DOI: https://doi.org/10.17605/OSF.IO/YFX89

Eligibility criteria

Types of evidence sources included original research reports, systematic reviews, narrative reviews, guidelines, and grey literature websites. Following removal of duplicates, screening of the sources of evidence to be included was performed by two or more reviewers according to the following inclusion criteria:

The diagnosis of SCD occurred in children aged ≤18 years of age.

Reports that included at least 50% of participants with a SCD diagnosis.

If representation of paediatrics or SCD diagnoses was fewer than 50%, but results were stratified, records could be included for review.

Reports investigating the musculoskeletal effects of SCD in children, and related management or interventional strategies.

Reports published between January 2000 and June 2024, inclusive.

The SCD diagnoses were eligible for inclusion as outlined by the MeSH term ‘Spinal Cord Diseases’, such as traumatic injuries and non-traumatic causes like myelitis or tumour. Therefore, reports that focused on conditions that do not qualify as an acquired SCD, e.g., spinal dysraphism, were not included. Furthermore, conference abstracts that had insufficient data to extract, reports discussing acute management of the SCI, and reports discussing the methodology of surgical management procedures were excluded. To minimize potential bias, no language restrictions were applied.

Information sources

The record selection process involved searching MEDLINE OVID, Excerpta Medica Database (EMBASE), and PubMed. These were selected due to their broad coverage of material pertaining to medicine and life sciences, whilst the grey literature information sources included government or institutional documents and pamphlet-style guidelines. Reference lists of similar reports were cross-checked to find records in addition to the OSF-registered protocol. Grey literature websites included were Google Scholar, System for Information on Grey Literature in Europe, the website of the American Spinal Injury Association, and the website of the International Spinal Cord Society.

Search

A scientific librarian-assisted search was designed, and JE built and performed the search in the included databases. An example of the electronic search for PubMed database, which was also adapted for EMBASE and MEDLINE OVID code, is available in Appendix A. The search was originally conducted on July 1, 2024, and a subsequent search including all languages was conducted on March 5, 2025.

Selection of sources of evidence

Three reviewers (JE, MG and AS) performed the screening – at both ‘Title and Abstract’ and ‘Full Text’ screening stages, JE screened every record, while MG and AS shared the records as reviewer two. Each reviewer independently screened records, and if any conflicts arose, these were resolved by consensus.

Data charting process and extraction

Covidence, which is an online software tool designed to support the systematic or scoping review process, was used for the entire screening and extraction process. It facilitates the separate screening of titles and abstracts from full texts, enables independent data extraction, and provides a process to reach consensus, which minimizes the risk of bias.²⁵

Data extracted from sources of evidence were charted using a data extraction form built in Covidence. The form was tested before its use. Data extraction was conducted independently: data from each included report was extracted by two independent reviewers as per the screening protocol, whereby JE extracted data from every report, while MG and AS each extracted data from half of the reports as reviewer two. The data obtained from both reviewers was then compared within Covidence by a single reviewer, and the confirmed data was exported to Microsoft Excel for descriptive analysis.

Data items

The variables gathered were General Information, Methods, Participants, Outcomes and Key Findings. General Information included sub-variables: Title, Year of Publication, Author Contact Details, and Country. Methods included sub-variables: Aim, Study Design, Start and End Dates, Funding Sources, and Conflicts of Interest. Participants included sub variables: Population Description, Inclusion and Exclusion Criteria, Recruitment Method, and Total Number of Participants.

Synthesis of results

Data extracted from each source of evidence were analysed descriptively and summarised into tabular format. The reports included were organised into separate categories based on the type of outcomes discussed. To achieve this, the key findings from sources of evidence were summarised and coded for descriptive qualitative content analysis. The main outcomes or keywords were used to identify whether the findings were reporting primarily biological, functional, or interventional conclusions. Sources of evidence were then grouped into the categories Physiological Parameters, Musculoskeletal Complications or Interventions based on what the main outcomes were exploring.

Results

Search

The combined searches resulted in a total of 6042 records, with the original search returning 6015, and the subsequent search returning 27. Embase retrieved 4488 records, Medline returned 1314 records, PubMed yielded 202 and a search of grey literature revealed 38 additional records, from reference lists, Google Scholar, the American Spinal Injury Association website, and the International Spinal Cord Society website. Following removal of duplicates and screening of ineligible records, assessment of 249 full text articles resulted in 45 reports eligible for inclusion. The sources of evidence were acquired, screened and extracted as summarised in Figure 1, including all relevant reasons for exclusion.

Figure 1.

PRISMA for scoping reviews flowchart of records obtained from multiple information sources, generated in covidence.

There were 10 cross-sectional studies, nine retrospective reviews of medical records, six case series, four narrative reviews, four randomised controlled trials, three non-randomised experimental studies, two systematic reviews, two case reports, and one each of a case-control study, cohort study, book chapter, conference task force, and guideline document. Seventeen studies received no funding, 16 were supported by grants from Shriners Hospitals for Children, 10 were funded by independent foundations and charities, and two studies were supported by both independent grants and a Shriners Hospitals for Children Grant, as indicated in Tables 1, 2, and 3.

Table 1.

Theme: Physiological parameters.

General Information	Methods		Participants	Primary outcomes	Key findings
Authors Year Country Citation	Aim	Study design	Population number	Primary outcomes	Key findings
Atkinson et al. 2019 United States*²⁶	To assess the capacity for residual muscle activation below the lesion in the developing and injured nervous system utilizing neurophysiological assessment methodology.	Cross sectional study	Children under 15 with spinal cord injury; N = 24 SCI	Electromyography	Spinal muscle activation occurs in children with spinal cord injuries that doesn’t occur normally.
Biggin et al. 2013 Australia*²⁷	To quantify regional changes in BMD, bone morphology and bone/muscle geometry in children following SCI using pQCT.	Cross sectional study	Children with cervical or thoracic SCI; N = 19	pQCT: BMD, Stress Strain Index, Total CSA, Cortical CSA, Muscle CSA, Total BMC, Cortical BMC and Diaphyseal circularity	Several bone parameters are reduced in children following a spinal cord injury diagnosis. Trabecular bone is more susceptible to decreasing BMD than cortical bone, at both radius and tibia. Bone geometry changes following spinal cord injury in non-ambulant patients. Weight-bearing increases bone mineral parameters and muscle CSA.
Coupaud et al. 2012 United Kingdom *²⁸	To identify the time point(s) at which BMD and other bone parameters fall below the normal range at fracture-prone sites in the absence of any intervention, and to investigate the potential for patient-specific predictive modelling of bone loss.	Case series	Inpatients of the Queen Elizabeth National Spinal Injuries Unit with SCI diagnosis; N = 4 paediatric	pQCT: Trabecular BMD, Total BMD, BMC and Total bone CSA	Bone parameters decrease rapidly throughout the first year of diagnosis, and more research is needed to ascertain when a new steady-state of bone mineral parameters is reached.
Curley et al. 2022 United States²⁹	To describe the relationship between the degree of neurologic deficit, bone and lean muscle mass, functional performance, and fracture occurrence in children with acute flaccid myelitis.	Retrospective review of medical records	Children <21 diagnosed with acute flaccid myelitis at a single centre; N = 79	DXA: BMC, BMD, Total lean mass and Fracture rate	Low BMD and mass is extremely common in children with acute flaccid myelitis. Muscle mass and bone mass are closely related and decrease simultaneously following diagnosis. Low bone mass may predict likelihood of pathological fractures.
Lauer et al. 2007 United States^⁸	To report on the BMD of the hip, distal femur, and proximal tibia in children with SCI of at least 1-year duration and before skeletal maturity.	Case series	Children with spinal cord injury at Shriners Hospital; N = 28	DXA: BMD values at the Total hip, Femoral neck, Greater trochanter, Ward's Triangle, Distal femur Proximal tibia	BMD is significantly decreased in the hip and knee in children with spinal cord injury. BMD decreases further in patients with higher spinal cord injuries and longer injury durations.
Liu et al. 2008 Australia³⁰	To document the serial changes in BMD following paediatric spinal cord injury.	Case series	Children with spinal cord injury (at C3-T12, median age 5.3y); N = 18	DXA: BMD and Lean tissue mass	Bone and muscle parameters decreased rapidly within 12 months of diagnosis, reaching a steady state sooner than adult counterparts.
Liusuwan et al. 2007 United States^³¹	To compare resting energy expenditure and body composition in patients with spinal dysfunction to able-bodied controls (normal weight and overweight) and examine relationship between resting energy expenditure and total lean mass in these groups.	Cross sectional study	Children with spinal cord dysfunction (traumatic SCI and spina bifida) and able-bodied controls (normal weight and overweight); N = 33 SCI	Body Mass Index; DXA: Lean tissue mass, Fat mass, Fat percentage and Resting energy expenditure	Patients with spinal cord injuries have significantly reduced fat and lean mass compared to control groups. While body fat percentage was lower in patients with spinal cord injuries compared to spina bifida and overweight controls, it was higher than normal weight controls. When adjusted for lean mass, resting energy expenditure was not significantly different between SCI subjects and control groups.
McDonald et al. 2007 United States^³²	To determine the body composition of adolescents with spinal cord injury and to assess whether established cutoff values for obesity determined by body mass index are valid for this population.	Cross sectional study	Children with spinal cord dysfunction (traumatic SCI and spina bifida) and able-bodied controls (normal weight and overweight); N = 60 SCI	Body Mass Index; DXA: Lean tissue mass, Fat mass and BMC of bodily compartments including arm, leg, trunk and total body	There were no differences in lean tissue mass, fat or BMC between paraplegics and tetraplegics of total body measurements, but there were regional differences. Children with paraplegia had higher lean tissue, fat and BMC in the arm, more fat in their legs, and higher lean tissue and BMC in their trunks.
Scott et al. 2006 United States^*³³	To investigate the effects of SCI on the contractile properties and force-frequency relationship of the paralysed human quadriceps femoris muscle.	Case control study	N = 26; 13 motor complete SCI adolescent patients and 13 matched able-bodied controls	Primary measures: Peak twitch force and fatigue ratios of quadriceps femoris, assessed by computerized dynamometer	SCI quadriceps muscle displayed lower peak twitch force and lower fatigue ratios, therefore is weaker and less resistant to fatigue than control muscle. Clinical findings related to stimulation frequencies that should be used to activate muscle during FES or training of paralysed muscles.
Scott et al. 2007 United States^*³⁴	To examine the electrically elicited force responses of the paralysed quadriceps femoris muscles of persons with SCI.	Non-randomised experimental study	N = 13; Adolescents with motor complete SCI	Isometric quadricep muscle performance was tested using 6-pulse Constant Frequency Trains, Variable Frequency Trains, and Doublet Frequency Trains delivered at mean frequencies of 10, 20, 33, 50, and 100 Hz, in both non-fatigued and fatigued conditions	Stimulation patterns that increase the force response in non-paralysed muscle do not do so in paralysed muscle. The force generated in paralysed quadriceps muscles by variable and doublet frequency trains depends on the frequency of stimulation, whether muscle is fatigued or not, and the force measure examined. This suggests that for patients with SCI, variable frequency trains will be most useful to increase peak force using frequencies <10 Hz in non-fatigued muscles and <20 Hz in fatigued muscles.
Widman et al. 2007 United States^³⁵	To assess upper extremity strength and aerobic fitness in a population of adolescents with mobility impairment due to SCI and spina bifida and to compare their values to those of a group of able-bodied adolescents.	Cross sectional study	Children with spinal cord dysfunction (traumatic SCI and spina bifida) and able-bodied controls (normal weight and overweight); N = 19 SCI	Anthropometrics (height, weight, body composition); Strength – dynamometer; Aerobic fitness – arm ergometer	Shoulder extension and flexion strength, as well as aerobic capacity, were significantly reduced in children with spinal cord injury compared to able-bodied controls.
Zebracki et al. 2013 United States^³⁶	To assess the incidence of vitamin D deficiency in youth with SCI.	Cross sectional study	Youth with SCI aged 3-21; N = 82	Serum vitamin D levels	Vitamin D insufficiency or deficiency were very common in children with spinal cord injury, with adolescents being more deficient than other age groups. Monitoring of vitamin D levels should be routine in this population.

Table 1: Reports of investigations into paediatric spinal cord disorders with a focus on physiological parameters. ^{^}Reports funded by grants from Shriners Hospital for Children; *reports funded by various independent foundations/charities/institutions. Abbreviations: Bone mineral content (BMC); Bone mineral density (BMD); Cross sectional area (CSA); Dual x-ray absorptiometry (DXA); Functional electrical stimulation (FES); Peripheral quantitative computed tomography (pQCT); Spinal cord injury (SCI).

Table 2.

Theme: Musculoskeletal complications.

General Information	Methods		Participants	Primary outcomes	Key findings
Authors Year Country Citation	Aim	Study design	Population number	Primary outcomes	Key findings
Bergstrom et al. 2003 United Kingdom³⁷	To assess the relation of the type of spinal fracture and its magnitude of distortion to the subsequent long-term development of the spinal column in childhood onset SCI.	Cross sectional study	Adults with paediatric-onset SCI; N = 76	Spinal deformities analysed were scoliosis, lordosis and kyphosis	The formation of scoliosis and lordosis following SCI is not caused by the fracture to the spine itself. Kyphosis formation may correlate with spinal fracture sites, but other mechanisms underlying deformity formation need to be explored.
Hwang et al. 2014 United States and Canada*³⁸	To determine longitudinal changes in the occurrence of medical complications in adults with paediatric-onset spinal cord injury.	Cohort study	Adults with paediatric-onset SCI; N = 431	Musculoskeletal medical complications analysed: Spasticity requiring medication and Bone fracture	Spasticity is highly prevalent in paediatric spinal cord injuries and is associated with tetraplegia. Fractures are less common but occur regardless of injury level.
Kulshrestha et al 2017 United Kingdom⁷	To determine the frequency of common long-term complications in patients sustaining spinal injury in childhood (0–18 years) and who were followed up at a single dedicated spinal injuries centre in the United Kingdom.	Retrospective review of medical records	Long term paediatric-onset SCI patients at a single dedicated spinal injuries centre in the United Kingdom; N = 69	Musculoskeletal complications included: Scoliosis and spasticity	Scoliosis and spasticity rates increase with increasing injury duration.
Kulshrestha et al. 2020 United Kingdom¹¹	To identify predictors of developing clinical scoliosis and compare between traumatic and neurological aetiologies of SCI.	Retrospective review of medical records	Patients with paediatric onset of SCI (<18); N = 62	Age at injury; Injury aetiology; Scoliosis development	Age at diagnosis was the only predictive factor of scoliosis development, with patients younger than 14.6 years having greater likelihood.
Maharaj et al. 2020 Australia³⁹	To overview the rehabilitation of children with spinal cord injury.	Book chapter	Children with spinal cord injury	Medical issues and Musculoskeletal issues	Scoliosis, spasticity, hypercalcemia, pathological fractures and hip dysplasia are common in the paediatric spinal cord injury experience. External devices and surgery are common management approaches for scoliosis, whilst upright weight-bearing can increase bone parameters and prevent fractures.
McCarthy et al. 2004 United States⁴⁰	To verify the incidence and degree of hip dysplasia in children with SCI, and to determine the association between age of injury and hip dysplasia.	Retrospective review medical records	Children with spinal cord injury; N = 62	Incidence and degree of hip dysplasia; History of hip or spine surgery; Pelvis radiographs - for migration index and medial joint space measurement	Hip dysplasia is very common among children with spinal cord injury. Chances of developing hip dysplasia in some capacity increase if diagnosis occurs before 10 years of age.
Meng et al. 2023 China*⁴¹	To determine the incidence and influencing factors of hip subluxation in children after SCI.	Retrospective review of medical records	Children with spinal cord injury; N = 146	Migration percentage and Acetabular index	Twenty-eight (19.2%) children had hip subluxation. The incidence of hip subluxation increased with the injury duration, with more than 50% occurring after 3 years. The Acetabular Index decreased with age. Migration Percentage and Acetabular Index in subluxated and normal hips were positively correlated. Children with injury age at or below 6 years, complete injury, and flaccid lower extremities had a significantly higher proportion of hip subluxation. There were no statistically significant differences in sex and injury level. Authors suggest regular follow-up is necessary to track structural changes in the hips in children with SCI.
Mulcahey et al. 2013 United States^¹²	To determine whether neurological level, motor score, and injury severity are strong predictors of neuromuscular scoliosis.	Cross sectional study	Children diagnosed with spinal cord injury who also have neuromuscular scoliosis; N = 217	Injury severity (complete vs incomplete); American Spinal Injury Association Impairment Scale classification; Age at injury; Neurological level (tetra/para) and Scoliotic curve/Cobb angle	Age at diagnosis was the only measured parameter that may indicate scoliosis development, with children under 12 at increased scoliosis risk.
Riklin et al. 2003 Switzerland⁴²	To assess (i) the incidences of deep vein thrombosis and heterotopic ossification in patients with SCI at the Swiss Paraplegic Centre Nottwil; (ii) the interval between the event of SCI and the diagnosis of these complications; and (iii) to examine mechanisms of interaction between deep vein thrombosis and heterotopic ossification.	Retrospective review of medical records	Patients admitted to the Swiss Paraplegic Centre with spinal cord injury; N = 4 paediatric	Clinical files were reviewed for incidence of heterotopic ossification	Heterotopic ossification is an extremely rare occurrence in adult spinal cord injury, and even more so in paediatric spinal cord injury. It is associated with physiological parameters of non-infectious inflammation.
Schottler et al. 2012 United States^¹⁴	To describe injury-related factors, demographic information, and the incidence of secondary complications that develop in children who sustained an SCI at 5 years of age and younger.	Retrospective review medical records	Children with spinal cord injuries obtained at 5 years 11 months or younger; N = 159	Demographic and injury-related factors included age at injury, aetiology, level of injury, American Spinal Injury Association Impairment Scale, and SCIs without radiological abnormalities. Musculoskeletal complications studied were: Scoliosis, Hip dysplasia and Spasticity	Scoliosis and hip dysplasia are highly prevalent in children with spinal cord injury and are associated with younger age at diagnosis. Ambulant patients were less likely to have severe scoliosis or hip dysplasia. Spasticity is also highly prevalent and associated with tetraplegia and incomplete injuries.
Suresh et al. 2022 United States⁴³	To describe factors that may predispose certain patients with acute flaccid myelitis to developing scoliosis over time.	Retrospective review of medical records and patient follow up	Children with acute flaccid myelitis diagnosis; N = 56	Presence of scoliosis; Ventilator dependence; Limbs affected; Ambulation status; Manual Muscle Testing score; Physical Abilities and Mobility Scale; Level of SCI	Scoliosis is highly prevalent in children with acute flaccid myelitis. It is associated with non-ambulation, extensive thoracic cord involvement and ventilator dependence. It is also likely to occur alongside other complications such as hip dysplasia and contractures.
Vogel et al. 2002 United States^¹³	To determine the associations between musculoskeletal and neurological complications and demographic and SCI-related factors.	Cross sectional study	Adults with spinal cord injury onset during childhood (0–18); N = 216	Prevalence of musculoskeletal complications since injury: Fractures, Scoliosis, Heterotopic ossification, Hip dislocation or contractures, Ankle contractures, Elbow contractures and Spasticity	Scoliosis was present in 40% of total participants, and hip dysplasia was present in 17%, both with greater likelihood of being present in children diagnosed before 12 years of age. Hip contractures, heterotopic ossification, spasticity and pathological fractures are also common occurrences and considerations of paediatric spinal cord injury.
Vogel et al. 2011 United States^⁴⁴	To describe outcomes of participation, life satisfaction, and medical complications as a function of impairment in adults with paediatric-onset spinal cord injury.	Cross sectional study	Adults who sustained paediatric SCI; N = 410	Education; Employment; Independent living anddriving; Marriage; Participation; Medical complications; Health-related quality of life; Global life satisfaction; American Spinal Injury Association motor score; Functional Independence Measure motor scores	Children with spinal cord injuries have a high prevalence of medical complications that extend over a longer period compared to adult counterparts. Muscle spasms, bone fractures and joint pain were complications of long-term concern in this study.

Table 2: Reports of investigations into paediatric spinal cord disorders with a focus on Musculoskeletal Complications. ^{^}Reports funded by grants from Shriners Hospital for Children; *reports funded by various independent foundations/charities/institutions. Abbreviations: Spinal cord injury (SCI).

Table 3.

Theme: Interventions.

General Information	Methods		Participants	Primary outcomes	Key findings
Authors YearCountry Citation	Aim	Study design	Population number	Primary outcomes	Key findings
Betz et al. 2001 United States^⁴⁵	To emphasise the importance of hip stability in patients when applying FES.	Case report	5-year-old child with T4 SCI observed until age 13; N = 1	Hip radiographs	FES should not be used in children with hip dysplasia following spinal cord injury unless surgical reconstruction is performed.
Boyce et al. 2014 United States*⁴⁶	To review current literature regarding bisphosphonate treatment in children with disabilities.	Narrative review	Various childhood conditions associated with osteoporosis and impaired mobility	Assessment of BMD in children; Conditions with impaired mobility – SCI; Treatment of childhood osteoporosis; Bisphosphonate treatment in children	DXA is the current gold standard for bone assessments in children. Bisphosphonate use in children with osteoporotic conditions is safe and efficacious, but lacking in quality evidence and long-term investigations.
Castello et al. 2012 United States*⁴⁷	To examine the effect of FES cycling on BMD and quality of life in children and adolescents with SCI.	Non-randomised experimental study	Children and adolescents with spinal cord dysfunction (<18); N = 6	DXA (BMD); PedsQL (Quality of life)	FES may increase BMD and quality of life, but results are lacking power.
Johnston et al. 2003 United States^⁴⁸	To evaluate the effects of FES applied to children with incomplete SCI 1 to 3 years post-injury to augment walking.	Case series	Children with incomplete SCI; N = 3	Improvements (with FES on and FES off) in: 1. Manual muscle test scores of all stimulated muscles 2. Energy cost of walking; walking distance; walking speed; step length 3. Joint kinematics: pelvic rotation; pelvic tilt	FES was efficacious in children with incomplete injuries to assist muscle stimulation and support upright ambulation.
Johnston et al. 2008 United States^⁴⁹	To report the outcomes of a 6-month at-home cycling program for 4 children with SCI.	Case series	N-4; Convenience sample of larger randomised clinical trial (Johnston et al. 2011)	DXA: BMD at hip, distal femur, proximal tibia; Magnetic resonance imaging: quadriceps muscle volume; Electrically stimulated strength of the left quadriceps; Spasticity of the quadriceps and hamstrings muscles; Heart rate and oxygen consumption	For both children who cycled with FES for 6 months, there were improvements in femoral neck, distal femur and proximal tibia BMD, muscle volume, and muscle strength. Similar findings were seen in only one of the passive cycling children, which may represent a ceiling effect for the influence of passive cycling on BMD.
Johnston et al. 2009 United States^⁵⁰	To examine the effects of a cycling program on hip subluxation in children with SCI.	Randomised controlled trial	Children with SCI at C4-T11, aged 5–13 years; N = 30	Radiographs	FES cycling, passive cycling and electrical stimulation is safe to use in children with hip dysplasia in SCI.
Johnston et al. 2011 United States^⁵¹	To determine the effect of cycling, electrical stimulation, or both, on thigh muscle volume and stimulated muscle strength in children with SCI.	Randomised controlled trial	N = 30; (N = 24 with muscle MRI data and 27 with stimulated strength data)	Magnetic resonance imaging to assess muscle volume; Computerized dynamometer to assess muscle strength testing	Children receiving either ES exercise experienced changes in muscle size, stimulated strength, or both. Quadricep volume was different between groups but not hamstring, with ES group gaining more quadricep volume compared to both FES cycling and PC. Within groups, FES cycling and ES both had increased quadricep volume from baseline. For stimulated strength, FES cycling gained more strength in quadriceps than PC, and within groups FES cycling was the only group to significantly see increased strength from baseline, with ES trending towards significance. FES cycling had greater strength changes while ES had greater volume changes.
Johnston et al. 2013 United States⁵²	To discuss the issues of decreased muscle mass and metabolic syndrome in paediatric SCI.	Narrative review	Literature on children with SCI and spinal cord dysfunction	The musculoskeletal issues in children with SCI and spinal cord dysfunction discussed: Decreased muscle mass and Increased risk of fractures	Exercise activities to increase muscle mass and fitness may be beneficial for increasing bone and muscle parameters to prevent musculoskeletal complications, but long-term investigations are lacking.
Keller et al. 2021 United States*⁵³	To establish the safety and feasibility of spinal cord transcutaneous stimulation as a potential therapeutic approach for upright sitting posture in children with SCI.	Non-randomised experimental study (within-subjects repeated measures design)	Children with chronic SCI at cervical or thoracic level and aged 3–14 years; N = 8	Acute effects of spinal cord transcutaneous stimulation on sitting posture: Compared flexion/extension angles at 3 spinal regions (L5S1, PelvisT8, and T8Head) during baseline, a volitional attempt to sit up, and spinal cord transcutaneous stimulation	Transcutaneous stimulation of spinal cord is safe and efficacious for use in children with spinal cord injury to support upright posture and trunk muscle engagement.
Lauer et al. 2011 United States^⁵⁴	To determine the effect of cycling and/or ES on hip and knee BMD in children with SCI.	Randomised controlled trial	Children with C4-T11 SCI aged 5–13 years; N = 30	DXA: BMD values at the Hip, Distal femur and Proximal tibia	BMD was not significantly affected by FES cycling, PC or ES interventions.
Ma et al. 2022 China*⁵⁵	To explore the immediate and long-term effects of robotic-assisted gait training on the recovery of motor function and walking ability in children with thoracolumbar incomplete SCI.	Randomised controlled trial	Children with thoracolumbar incomplete SCI; N = 20	10-metre Walk Test was used to calculate the Self-selected Walking Speed and Maximum Walking Speed; Six-Minute Walk Distance; Lower Extremity Motor Score; Balance and postural control, as measured by a centre of pressure calculation; Walking capabilities, as measured by the Walking Index for Spinal Cord Injury II; Energy expenditure, as measured by the physiological cost index	The experimental group underwent robotic assisted gait training utilizing Lokomat Pro Pediatric version. There were statistically significant improvements in all outcome measures in the experimental group compared to the control group. However, these effects were not maintained at follow-up. The experimental group formed a new gait pattern, and their immediate motor function and walking ability were significantly improved, but long-term efficacy is lacking.
Mayson et al. 2014 Canada⁵⁶	To review the evidence on FES cycling intervention in youth with SCI.	Systematic review	Reports describing FES cycling for children with SCI	Body structure and function: BMD, oxygen consumption, forced vital capacity, muscle volume, hip migration index, resting heart rate, Pediatric Quality of Life Inventory	FES cycling is a safe intervention method in children with SCI. However, increases in BMD were not significant, and while positive effects were observed on muscle parameters, results were not readily generalizable.
Mehta et al. 2004 United States^⁵⁷	To evaluate their patient population for the development and progression of spinal deformity after SCI and the impact of bracing vs non-bracing in the development of spinal deformity after SCI.	Retrospective review of medical records	Children with cervical or thoracic SCI Aged 2–13; N = 123	Spinal radiographs for Scoliosis description and Cobb angle	Early bracing was effective in patients with scoliotic curves below 20° in preventing the need for surgical intervention but was ineffective for those with curves over 41°. Early surgical intervention is recommended for those patients with severe curves over 41°.
Ooi et al. 2012 Australia⁵⁸	To report the effect of zoledronic acid on BMD in a child with non-traumatic SCI.	Case report	N = 1; 12yo male diagnosed with incomplete SCI due to necrotizing myelitis at 8.1 years old.	DXA: BMC, areal BMD; pQCT: BMC, volumetric BMD, cortical CSA, cortical thickness and SSI; Bone turnover markers: calcium, phosphate, alkaline phosphatase, parathyroid hormone, 25-Hydroxyvitamin D, Osteocalcin, Calcium: creatinine ratio and Deoxypyridinoline: creatinine ratio	Patient was commenced on zoledronic acid 1 month after pathological fracture of right humerus at 9.5 years of age. Bone turnover decreased, with both formation and resorption markers reduced following treatment. DXA showed improved total body and lumbar spine BMC and areal BMD. pQCT showed improvement in metaphyseal (trabecular) and diaphyseal (cortical) BMC, volumetric BMD, cortical thickness and CSA, resulting in increased tibial SSI, after 18 months of treatment. Radial SSI remained unchanged. In the growing skeleton post-SCI, zoledronic acid proves potentially effective in improving bone health, by reducing bone turnover rates and increasing bone strength, trabecular bone, cortical density and CSA.
Papapoulos 2011 The Netherlands⁵⁹	To discuss the viability of introducing bisphosphonates into standard therapy for children with chronic conditions and secondary osteoporosis.	Narrative review	Children with chronic conditions causing secondary osteoporosis	Topic headings: Childhood osteoporosis; Management issues; Bisphosphonate use in children; Bisphosphonate use in children with secondary osteoporosis	While bisphosphonates may be safe and effective for use in children with osteoporotic conditions, extensive quality evidence is lacking.
Parent et al. 2010 Canada*⁶⁰	To identify the unique features associated with paediatric spinal cord injury with the intention of determining the most effective spinal stabilization methods and identifying the optimum treatment for post-traumatic spinal deformity in paediatric patients with a SCI.	Systematic review	Children with spinal cord injury 17 years or younger	Research questions: 1. What is the most effective means to achieve spinal stabilization in paediatric patients with a SCI? 2. What is the most effective treatment of post-traumatic spinal deformities in paediatric patients with a SCI?	Most treatments are based on the experience of adult spinal cord injury, and no randomised, prospective studies in children exist investigating treatment and prevention of neuromuscular deformities.
Parisini et al. 2002 Italy⁶¹	To evaluate clinical and radiologic findings and the effectiveness of conservative versus surgical treatment at long-term follow-up for children and adolescents with spinal fractures.	Case series	Children and adolescents with spinal injuries; N = 11 SCI	Spinal radiographs reviewed for presence of scoliosis/kyphosis, associated with type of treatment (conservative vs surgical)	Spinal deformities occur in over 90% of paediatric spinal cord injury patients, and conservative vs. surgical management of the fracture is dependent on the nature of spinal stability. Early surgical treatment appears to be important in treating both unstable fractures and preventing deformities in children with spinal cord injury.
Ruppert et al. 2022 United States⁶²	N/A	Guidelines for equipment and orthoses to augment or replace lower extremity function	People with spinal cord injury	Considerations for orthotic use included: Extremity musculature, scoliosis, pelvic obliquity, hip subluxation/dislocation, fracture, amputation, spasticity, contractures, upright positioning and gait	Instrumentation to support upright positioning and mobility and prevent musculoskeletal complications in lower limbs was explored. Orthoses include stander; ankle foot orthosis; knee ankle foot orthosis; hip knee ankle foot orthosis; reciprocating gait orthosis; FES surface stimulation systems; hybrid systems; and robotics such as exoskeletons.
Sadowsky 2023 United States⁶³	To discuss the relationship between muscle mass and functional ability in children with neurologic injury and propose muscle-focused clinical approaches to support this population.	Narrative review	Children with spinal cord related paralysis	Evaluation methods for muscle mass: Skin fold, waist circumference, Body Mass Index, ultrasound, bio-electric impedance analysis, creatine excretion, neutron activation, DXA, computed tomography, and magnetic resonance imaging. Strategies to increase muscle mass and reverse sarcopenia: Exercise and diet	There are no standardized methods for objective measurement of muscle mass in children because of ongoing changes in body composition during childhood. Risk factors for sarcopenia include lack of activity or exercise, hormone and cytokine imbalance, and abnormal protein synthesis related to poor ability to contract a muscle against a mechanical load. Strategies to increase muscle mass and reverse sarcopenia include exercise and diet. Activity-based restorative therapies, low load resistive training coupled with blood flow restriction, and FES may enhance exercise therapies for children with SCI. Protein intake is important in maintaining muscle health, but studies are lacking in children with SCI. Creatine monohydrate has been documented to have anabolic potential and used with exercise to improve muscle strength and volume, and nicotinamide riboside may be efficacious in sarcopenia.
Shuhart et al. 2019 United States⁶⁴	To update 34 official positions of the International Society for Clinical Densitometry.	Conference, task forces, and voting	Expert panels	Relevant topics: Proximal femur and 33% radius measures in paediatric patients, lateral distal femur measures in special populations, and use of vertebral fracture assessment in paediatric patients	DXA and pQCT are safe and useful for assessing bone health in children, but DXA is the current gold standard, with standardized guidelines for pQCT use lacking. Distal femur measurements may also be useful in assessing fracture risk in non-weightbearing children.

Table 3: Reports of investigations into paediatric spinal cord disorders with a focus on Interventions. ^{^}Reports funded by grants from Shriners Hospital for Children; *reports funded by various independent foundations/charities/institutions. Abbreviations: Bone mineral content (BMC); Bone mineral density (BMD); Cross sectional area (CSA); Dual x-ray absorptiometry (DXA); Electrical stimulation (ES); Functional electrical stimulation (FES); Passive cycling (PC); Peripheral quantitative computed tomography (pQCT); Spinal cord injury (SCI); Strength strain index (SSI).

The majority of studies were conducted in North America (United States 29/45; Canada 2/45), and one was a multi-site study conducted in both countries (1/45). The remaining studies were conducted in the United Kingdom (4/45), Australia (4/45), China (2/45), Italy (1/45), Switzerland (1/45) and the Netherlands (1/45).

Examination of the included reports revealed three general types of conceptual approach. These included studies that investigated the Physiological Parameters, Musculoskeletal Complications or possible Interventions related to paediatric SCDs.

Physiological parameters

Twelve included reports were of investigations into various Physiological Parameters relating to the paediatric SCD experience (Table 1). These sources of evidence highlight that patients with SCD have significantly reduced bone mineral content (BMC), BMD, lean tissue mass and cross-sectional area (CSA),^8,27,32 abnormal muscle activation,²⁶ and reduced muscle strength,^33–35 compared to typically developing children. Cortical bone appears to be less likely to reduce in density than trabecular bone, and bone circularity changes appear to occur within the early months of diagnosis.²⁷ Two studies observed that these parameters decreased most rapidly throughout the first 12 months of diagnosis.^28,30 It was also observed that vitamin D insufficiency and deficiency are common within this population.³⁶ These losses of bone and muscle physiology parameters appear to be correlated with loss of weight-bearing ability and decrease further over time.^29,30

Musculoskeletal complications

Thirteen included reports were of investigations into various Musculoskeletal Complications associated with paediatric SCD (Table 2). The most common musculoskeletal complications associated with paediatric SCD included scoliosis, spasticity, hip dysplasia, hypercalcemia, fractures, contractures^{7,11–14,37–41,43,44} and, to a much lesser extent, heterotopic ossification.⁴² These effects are more profound in patients diagnosed during childhood, compared to those injured later in life.^{13,14,38–40,44} A key issue may be the lack of appropriate stress upon bones during critical periods of bone growth, on the journey to peak bone mass, as ambulant children have fewer complications associated with their condition. Ambulatory status, defined as those who are community ambulators, positively correlated with BMD in the femur, based on DXA assessment of the distal femur.²⁹ Furthermore, load-bearing in a standing frame (or better) attenuated the losses in trabecular density, cortical area, and muscle CSA. Mobile patients able to stand without a standing frame exhibited better tibial circularity scores than patients who could not, based on pQCT assessment of the tibia.²⁷ Independently ambulatory patients who walked with an assistive walking device or better were also less likely to have scoliosis.³⁹ Age at injury was highlighted as a risk factor for scoliosis and hip dysplasia, with children diagnosed pre-puberty being at greater risk.^{11,12,14,40,41} Complete injuries and flaccid paralysis were also noted to correlate with the development of hip subluxation.^14,41 Spasticity was associated with tetraplegia, and rates increase with injury duration.^7,14 It was also highlighted that scoliosis may arise from changes to motor control of the spine following injury, rather than the fracture of the spinal column itself.³⁷

Interventions

Twenty included reports were of investigations into various potential Interventions to assist in the treatment of paediatric SCD (Table 3). Several evidence sources explored the use of functional electrical stimulation (FES) in paediatric SCD and found it to be safe for use in children, but these studies often had small sample sizes and therefore lacked power.^{45,47–51,53,54,56} Most of these studies reported trends towards increases in BMD with FES.

It was also proposed that exercise interventions^52,63 to increase weight-bearing as well as dietary strategies to support muscle mass would also be of benefit for muscle and bone parameters. Some studies explored the use of robot-assisted exercise programs to facilitate muscle mass and walking ability, but long-term efficacy is unknown.^55,62

Pharmacological interventions included mostly bisphosphonate treatment,^46,58,59 which was reported as safe for use in children and used following fragility fractures on a case-by-case basis.⁵⁹

Two studies explored the utility of surgery or bracing to prevent paralytic scoliosis,^57,61 in which bracing was only effective in cases where scoliosis was less severe,⁵⁷ and early surgical intervention was recommended to prevent scoliosis development.^57,61

Discussion

Summary of evidence

This scoping review revealed several gaps in the literature regarding the musculoskeletal health and management in children with SCD. While it is well understood that musculoskeletal changes following SCD can differ in children compared to their adult-injured counterparts, the mechanisms underlying these differences are not known. The timeline of bone and muscle deterioration is not comprehensively understood, and the development of musculoskeletal complications such as spinal deformities should be investigated further. The prevalence of musculoskeletal complications following paediatric SCD have been documented, yet CPGs supporting musculoskeletal health are lacking and complications are generally treated on a case-by-case basis.

While the existing sources of evidence are important in the grand scheme of paediatric SCD research, there is an overwhelming dearth of high-quality evidence that could support the development of evidence-based CPGs. However, a recent report on CPGs for the management of autonomic dysfunction in SCD highlighted that lower-level evidence can be used to develop CPGs if there is consensus, and that is the only evidence available.⁶⁵ For example, based on the findings from this review, the first point to discuss for future guidelines for managing musculoskeletal health in paediatric SCD would be to alert clinicians to the high prevalence of these complications in these children compared to adults with SCD. This is a health issue that is often not considered during acute management and can be ignored in these early stages when other health complications are more pressing, yet the deterioration of musculoskeletal health can result in significant complications such as spinal deformities or fragility fractures. By the time these occur, they are too late to prevent and they negatively impact quality of life. Therefore, the findings of this scoping review could provide the basis for a similar undertaking to develop CPGs regarding musculoskeletal health for children with SCD. Implementation of preventative monitoring strategies may reduce the incidence of these complications, which in turn may reduce associated pain and increase quality of life.

The current standard for bone health assessment in paediatric SCD is DXA.^64,66 But while DXA is used to assess bone mineral parameters, often following a fragility fracture, it does not provide the best data by which to judge outcomes.^27,66 pQCT has superior resolution and assesses several meaningful bone health parameters that DXA does not, such as volumetric BMD, skeletal geometry, and bone strength, and distinguishes between trabecular and cortical bone.⁶⁷ However, while it has been utilised in some prospective studies, it is not used in routine clinical care for children with SCD due to insufficient paediatric reference data and technical issues pertaining to the positioning of the 4% scan.⁶⁸ The 4% site measures the trabecular bone at the metaphyseal region of the radius and tibia, which is proximal to the growth plate. This makes obtaining measurements at the same reference point within this growing population rather difficult.⁶⁸ Further studies are required to ascertain the utility of each imaging modality for the purposes of bone health monitoring in paediatric SCD. However, this concept of including musculoskeletal imaging assessments before pathological complications arise could help improve the care and management of bone health in this population.

In terms of potential interventions to promote musculoskeletal health in paediatric SCD, very few controlled studies have been performed. Of the 20 reports that discussed potential interventions, only eight involved prospective study designs, of which there were only five distinct cohorts – four of these reported multiple outcomes from the same cohort,^49–51,54 with the remaining four reporting on independent cohorts.^47,48,53,55 This highlights a significant lack of studies aimed at developing interventions to support musculoskeletal health in paediatric SCD. These studies, while often suggesting promising effects, lacked power due to small sample sizes.^47–49,53 Given the overall low prevalence of paediatric SCD, this may be a persistent issue; therefore, national and international collaborative research efforts may require consideration.

Bisphosphonates were the primary focus for pharmacological intervention.^46,58,59 They are used in adults and children to increase BMD and treat bone fragility conditions such as osteoporosis, as they increase bone mass and prevent resorption.⁶⁹ However, prospective studies to support routine clinical use are lacking.⁵⁹ Overall, interventions for musculoskeletal health are lacking, but quality intervention studies cannot be performed until more research is conducted within this population. For example, longitudinal studies exploring the timeline and mechanisms of bone deterioration²⁸ would help contribute to the foundation of knowledge of bone health in paediatric SCD that this scoping review highlights.

Limitations

A key observation from this scoping review revealed that nearly half of the evidence sources were supported by grants from one centre in the USA. Eighteen of the 45 reports included arose from research efforts by the Shriners Hospital for Children. However, this condition is not a phenomenon exclusive to the USA, and this large contribution by one centre to the research field may introduce bias. Corroborating data from other treatment centres outside of the USA, in both hospital and community centres, is very much needed due to potential effects of differing healthcare systems and to avoid potential bias in reporting.

Due to the breadth of available sources of evidence, it was challenging to standardise the information extracted from each reference. The varying methodologies and limited number of publications on this topic meant that uniform analysis of available literature was difficult. For example, while the recommendations from some of the studies included in this review may be useful and relevant for paediatric SCD, many of the techniques discussed were more related to the methods used for assessment of bone health in children in general, not specifically to children with SCD. The overall lack of studies performed on this topic meant that the published reports are difficult to compare and generalise to the entire population of paediatric SCD.

This is further emphasised by the aetiology focus of most of the included reports. While this scoping review has revealed the status of the literature landscape for musculoskeletal health in paediatric SCD, it appears that many studies include traumatic aetiologies only. Given that nearly two-thirds of the paediatric SCD population are represented by non-traumatic causes,^1,3,70 the lack of discussions of non-traumatic aetiologies in the literature means that the experience of over half of the paediatric population with SCD is not being adequately captured. Non-traumatic diagnoses result in heterogenous SCD experiences; the injuries to the spinal cord are often incomplete yet extensive, with damage commonly occurring across several spinal levels.⁷¹ While this may make it difficult to study this population, it should not be ignored.

Conclusions

This scoping review aimed to ascertain from the literature the structural and functional musculoskeletal changes and associated treatment strategies in paediatric patients with spinal cord disorders. Gaps highlighted included a lack of underlying mechanistic knowledge for the timeline of musculoskeletal deterioration and development of complications. This underscores the lack of available CPGs to support the management of musculoskeletal health in these children.

Implications of the findings for research, practice, and policy

Investigations into potential interventions to support musculoskeletal outcomes are imperative. What has been achieved to date has shown several potentially positive outcomes, but these studies are underpowered, thus their findings have not yet been translated into routine clinical care. Future studies further exploring the effects of standing and weightbearing interventions, electrical stimulation, and pharmacological strategies to manage musculoskeletal complications following paediatric SCD would be beneficial, however, it would be possible for CPGs to be produced if consensus can be reached. Therefore it is also recommended that paediatric SCD clinicians and researchers engage in discussions of the findings from this scoping review, to reach consensus on a set of guidelines based on current knowledge and evidence to date, thus improving the management of musculoskeletal complications for these children.

Footnotes

Acknowledgements

We thank Poh Chua from The Royal Children's Hospital library for her assistance building the database searches used in this study.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

ORCID iDs

Jamie Ellis

Peter Simm

Adam Scheinberg

Mary P Galea

Appendix A: Sample search strategy (PubMed)

#1. Title/abstract

“sci” OR “scd” OR “spinal-cord-injur*” OR “spinal-cord-disorder*” OR “spinal-cord-disease*”

#2. Title/abstract

“newborn*” OR “new-born*” OR “baby” OR “babies” OR “neonat*” OR “neo-nat*” OR “infan*” OR “toddler*” OR “pre-schooler*” OR “preschooler*” OR “kinder” OR “kinders” OR “kindergarten*” OR “kinder-aged” OR “boy” OR “boys” OR “girl” OR “girls” OR “child” OR “children” OR “childhood” OR “pediatric*” OR “paediatric*” OR “school-age*” OR “schoolage*” OR “schoolchild*” OR “schoolgirl*” OR “schoolboy*” OR “adolescen*” OR “youth” OR “youths” OR “teen” OR “teens” OR “teenage*”

#3. Title/abstract

“skeletal” OR “musculoskeletal” OR “fracture*” OR “scoliosis” OR “dislocation*” OR “contracture*” OR “bone*” OR “tibia” OR “radius” OR “femur” OR “ulna*” OR “hip” OR “pelvis” OR “paraplegi*” OR “quadriplegi*” OR “DEXA” OR “DXA” OR “dual energy x-ray absorptiometry” OR “pQCT” OR “peripheral quantitative computed tomography” OR “bisphosphonate*” OR “vitamin D” OR “bone mineral density” OR “muscle”

#4. Title/abstract

“longterm” OR “long-term” OR “repeat*” OR “serial” OR “longitudinal*” OR “follow-up” OR “followup” OR “cohort*” OR “retrospective*” OR “prospective*” OR “clinical-stud*” OR “clinical-articl*” OR “clinical-trial*”

#5. NOTNLM OR publisher[sb] OR inprocess[sb] OR pubmednotmedline[sb] OR indatareview[sb] OR pubstatusaheadofprint

#6. #1 AND #2 AND #3 AND #4 AND #5

Limit from year 2000 onwards

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