Abstract
Adolescent idiopathic scoliosis (AIS) a common spinal condition affecting adolescents. Though the etiology is still unknown, it is widely thought to have a multifactorial etiology and early diagnosis remains a significant challenge. The purpose of this study is to identify early vertebral morphological changes and patterns of spinal asymmetry in these at-risk individuals who later progress to adolescent idiopathic scoliosis. This was a retrospective study of patients treated for AIS between 1997 and 2017. We utilized two study groups, a group with immature onset of spinal asymmetry and a control group. Inclusion criteria for the immature onset group was defined by a Cobb angle between 10 and 40° diagnosed prior to the age of 12 with MRI scans and XRs available for review. Qualitative assessments observed for sagittal vertebral wedging, analysis of vertebral corner anatomy, spinal harmony, and sagittal balance. These findings were then qualitatively compared between groups. Twenty patients were included in this study, ten each in the immature onset and control groups. In the immature onset group, two patients had sagittal wedging, five had abnormal vertebral corners, nine did not have spinal harmony, and nine had negative sagittal balance, compared to none of the control patients having sagittal wedging, none having abnormal vertebral corners, all having spinal harmony, and nine having positive spinal balance. This pilot MRI study identifies qualitative vertebral morphological changes in patients who progress to AIS. Our findings suggest abnormal vertebral corner anatomy, sagittal wedging, and negative sagittal balance as potential early findings in patients who develop AIS.
Keywords: Adolescent idiopathic scoliosis, Hueter-Volkmann principle, Vertebral morphology, Relative anterior spinal overgrowth, Spinal asymmetry
1. Introduction
Scoliosis is a common spinal condition affecting children and adolescents.1 It is commonly described as non-idiopathic or idiopathic, with non-idiopathic scoliosis having a clear etiology, such as vertebral malformations or neuromuscular abnormalities, and idiopathic scoliosis having no clear etiology. Adolescent idiopathic scoliosis (AIS) affects those between 11 and 18 years of age and accounts for nearly 90% of idiopathic cases affecting children.1 It has an overall prevalence of 0.47–5.2%, yet despite this high prevalence, knowledge regarding the pathogenesis of AIS remains limited.2 Thus, AIS is most widely accepted as having a multifactorial etiology, being the result of a combination of genetic and biomechanical factors that predispose an immature spine to asymmetrical growth.3, 4, 5, 6
There are believed to be a few important factors that are at play in AIS. These include anthropology/bipedal gait, a natural susceptibility to deformity in the immature rapidly growing erect human spine, inherent torsion associated at the induction of deformity, biomechanics related to curve progression and the contribution of bone health. The synthesis of these multiple factors will allow for a more complete picture to be established and lead to a better understanding of why AIS occurs. This more in depth understanding of the etiology will aid in directing ways to optimize evaluation, treatments and therapies, especially early treatments with less invasive methods.
One theory behind the early development of AIS centers on the importance of proper sagittal alignment.7 This is particularly important during the early growth phase of the spine. The Heuter-Volkmann principle suggests that compressive forces result in accelerated closure of epiphyses and distractive forces result in delayed closure.8, 9, 10 Thus, a lack of adequate thoracic kyphosis in the sagittal plane would result in abnormal vertebral forces that could drive at-risk individuals into scoliotic deformities during spinal growth. This concept is also known as relative anterior spinal overgrowth (RASO), which has been previously identified as occurring in thoracic vertebrae of patients with AIS,11 as illustrated in Fig. 1. We hypothesize that these at-risk individuals who progress to AIS have early morphological changes of their thoracic vertebrae that can be identified with magnetic resonance imaging (MRI) prior to the severe progression of their curves.
Fig. 1.
Distribution of Proposed Loading Forces in a Normal and IS Affected Vertebra. The Hueter-Volkmann effect of asymmetric loading of axial forces on the thoracic vertebra creates RASO (relative anterior spinal overgrowth). RASO + inherent right torsion - growth = induction of scoliosis.
2. Methods
2.1. Study design and patient selection
Ethical approval was obtained from the Institutional Review Board prior to the initiation of this study. This was a retrospective observational study of patients who received their medical care at Lurie Children's Hospital. We utilized two groups, a study group with immature onset scoliosis and a control group with no known musculoskeletal disorders, age matched to the patients in the study group. Immature onset scoliosis was defined as a Cobb angle between 10 and 40° diagnosed prior to the age of 12. This allowed us the best opportunity to identify early vertebral morphological changes prior to curve progression. Patients were identified within the Lurie Children's Hospital's electronic medical record system between 1997 and 2017 and were required to have spinal MRIs performed prior to the age of 12. Patients were excluded if they had any associated non-idiopathic causes of their spinal deformity.
2.1.1. Qualitative assessments
We identified twenty total patients for this study, ten in the study group and ten in the control group. XR and MR images of the spine were then qualitatively reviewed for vertebral morphological changes. Qualitative assessments of vertebral morphology included identification of the presence or absence of sagittal vertebral wedging (scoliotic deviation associated with the vertebra and discs in all three planes), maintenance of vertebral corner morphology (shape and height of vertebra), spinal harmony (harmonious if spine has a continuous shape without abrupt change), and sagittal balance (front-to-back balance of spine with characteristic alignment). Four trained reviewers examined the imaging and discussed any uncertainties until a consensus was reached.
3. Results
3.1. Patient demographics
The average age of the patients in this study was 9.4 years of age (range 6–12) for both the study and control groups. There were 8 females and 2 males in the study group and there were 10 females in the control group. The average BMI was 16.68 kg/m2 in the study group and 19.53 kg/m2 in the control group.
3.2. Qualitative vertebral abnormalities
As seen in Table 1 and Table 2, two patients in the study group demonstrated sagittal wedging compared to no patients in the control group. Half (n = 5/10) of the patients in the study group lost their right-angled vertebral corners and were found to have more rounded to concave appearing corners compared to completely intact vertebral corners in the control group. 10% of the patients in the study group had spinal harmony compared to 100% of the control patients having spinal harmony. Finally, 90% of patients in the study group had negative spinal balance compared to 90% of the patients in the control group having positive spinal balance. Additional notable findings include coronal plane wedging seen in one of the patients in the study group compared to no coronal plane wedging seen in the control patients.
Table 1.
IS affected group qualitative observations from MR imaging.
| Patient # | Age | Gender | Sagittal Wedging Present (Y/N) | Vertebral Morphology in Tact (Y/N) | Spinal Harmony (Y/N) | Sagittal Balance Present (±) | Comments |
|---|---|---|---|---|---|---|---|
| 1 | 6 | F | N/A | N | N | negative | |
| 2 | 7 | F | Maybe (T6-T8) | Y | N | negative | |
| 3 | 8 | F | N | Y | N | negative | |
| 4 | 8 | M | Y | Y | N | negative | |
| 5 | 9 | F | N | Y | Y | negative | |
| 6 | 9 | F | N | N | N | negative | |
| 7 | 11 | F | N | N | N | negative | |
| 8 | 12 | F | Y | N | N | negative | Coronal wedging present |
| 9 | 12 | M | N | N | N | positive | |
| 10 | 12 | F | N | Y | N | negative |
Table 2.
Control group qualitative observations from MR imaging.
| Patient # | Age | Gender | Sagittal Wedging Present (Y/N) | Vertebral Morphology in Tact (Y/N) | Spinal Harmony (Y/N) | Sagittal Balance Present (±) | Comments |
|---|---|---|---|---|---|---|---|
| 11 | 6 | F | N | Y | Y | positive | |
| 12 | 7 | F | N | Y | Y | positive | spondylolisthesis |
| 13 | 8 | F | N | Y | Y | positive | |
| 14 | 9 | F | N | Y | Y | positive | |
| 15 | 9 | F | N | Y | Y | positive | |
| 16 | 10 | F | N | Y | Y | positive | |
| 17 | 10 | F | N | Y | Y | positive | |
| 18 | 11 | F | N | Y | Y | N/A | |
| 19 | 12 | F | N | Y | Y | positive | |
| 20 | 12 | F | N | Y | Y | positive | T-4-T6 superior endplate decreased |
4. Discussion
Adolescent idiopathic scoliosis is widely accepted as having a multifactorial etiology, resulting from the synergistic effects of biomechanical and external pressures on the immature spine with susceptible vertebrae and intervertebral discs.3, 4, 5, 6 This study suggests that these biomechanical pressures may result in early vertebral morphological changes that may be identified with XR and MR imaging early in the disease process, prior to severe curve progression.
Early biomechanical theories regarding the progression of spinal deformity discussed-- with little support-- the influence of hip abduction or adduction contractures resulting in pelvic asymmetry and unequal load of the spine.12,13 This asymmetrical loading of the spine is hypothesized to influence the development of scoliosis deformities. Early work by Roaf supports the importance of spinal asymmetry in the disease process by discussing the role of increasing compressive forces on the concavity of the deformity resulting in decelerated growth.14 Thus, with the combination of decelerated growth in the concavity of the deformity and resultant growth in convexity of the deformity, spinal growth can result in a “vicious cycle” of spinal deformity progression.8
The principle of constant pathologic pressure inhibiting endochondral longitudinal growth and reduced pressure resulting in accelerated growth is attributed to the Heuter-Volkmann or Depech effect.8, 9, 10 Work by Stokes et al. further supports this concept.8,9 He used biomechanical models to describe the role of differential forces on vertebrae and resultant influences on scoliosis curve progression. The clinical implication of these biomechanical theories suggests that there should be associated vertebral morphological changes when abnormal forces are present.
Keenan et al. investigated the hypothesis of vertebral morphological changes in AIS by observing coronal wedging deformities in patients with progressive scoliosis deformities.15 They found measurable changes in wedging, however there were no consistent changes found between patients with curves that progressed and those who did not. Our study found only a single patient with coronal wedging, however we did identify two patients with sagittal wedging compared to none in the control group. Newell et al. investigated the concept of relative anterior spinal overgrowth, which would influence the growth of spines in the sagittal plane.16 They found that patients with AIS have proportionally longer anterior columns compared to non-scoliotic controls. Basic science studies also support the idea of RASO. A histological study of the spinal growth plates in patients with AIS found significantly larger hypertrophic and proliferative zones in the anterior spinal column compared to the posterior column.17
Abnormal vertebral morphology also appears to be more prevalent in patients with AIS.18 Brink et al. noted significant vertebral asymmetry in patients with AIS. Findings from the current study support this finding as half of the patients who went on to develop AIS had abnormal vertebral morphology, while none did in the control group. This supports the concept that subtle morphological changes can be seen in the vertebrae of patients who go on to develop AIS.
Finally, the findings from this study support the growing evidence that sagittal balance plays an integral role in AIS development. Ninety percent of patients in this study who went on to develop AIS had a negative sagittal balance prior to curve progression, compared to 90% of control patients having positive sagittal balance. This suggests that early identification of negative sagittal balance should raise a clinician's suspicion for a developing scoliotic deformity.
This study has several inherent limitations. First, it included a limited sample size given the pilot nature of the study, which limits the ability to perform statistical analyses on the data. Additionally, the data represent a single point in time and cannot account for progressive changes in patients over time. Moreover, MR imaging is obtained with a patient lying supine, which should be noted when comparing our findings regarding sagittal balance to findings where the imaging is obtained with the patient standing upright.
5. Conclusions
This pilot MRI study identifies qualitative vertebral morphological changes in patients who go on to develop AIS. Our findings of negative sagittal balance, increased abnormal vertebral morphology and sagittal wedging in patients who develop AIS identify early morphological changes that can be identified with MRI. Our findings further support the role of the Heuter-Volkmann principle and RASO in the induction phase of early AIS.
Author contributions
Ayesha Maqsood and John F. Sarwark are credited for substantial contributions to the research design, analysis and interpretation of the data, drafting the paper and revising it critically, and approval of the final submitted version. Sohaib Z. Hashmi is credited with contributions to the analysis and interpretation of the data, revising the draft critically, and approval of the final submitted version. Matthew Hartwell is credited for revising the draft critically and approval of the final submitted versions.
Declaration of competing interest
The authors have no conflict of interests to disclose.
Contributor Information
Ayesha Maqsood, Email: amaqsood@luriechildrens.org.
Sohaib Z. Hashmi, Email: sohaibzhashmi@gmail.com.
Matthew Hartwell, Email: matthew.hartwell@northwestern.edu.
John F. Sarwark, Email: jsarwark@luriechildrens.org.
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