Journal of Clinical Medicine Article Ossification and Fusion of the Vertebral Ring Apophysis as an Important Part of Spinal Maturation Lorenzo Costa , Steven de Reuver , Luc Kan, Peter Seevinck, Moyo C. Kruyt, Tom P. C. Schlosser and René M. Castelein * Department of Orthopaedic Surgery, University Medical Center Utrecht, 3584CX Utrecht, The Netherlands; [email protected] (L.C.); [email protected] (S.d.R.); [email protected] (L.K.); [email protected] (P.S.); [email protected] (M.C.K.); [email protected] (T.P.C.S.) * Correspondence: [email protected]; Tel.: +31-88-755-4578; Fax: +31-30-251-0638 Abstract: In scoliosis, most of the deformity is in the disc and occurs during the period of rapid growth. The ring apophyses form the insertion of the disc into the vertebral body, they then ossify and fuse to the vertebrae during that same crucial period. Although this must have important implications for the mechanical properties of the spine, relatively little is known of how this process takes place. This study describes the maturation pattern of the ring apophyses in the thoracic and lumbar spine during normal growth. High-resolution CT scans of the spine for indications not related to this study were included. Ossification and fusion of each ring apophysis from T1 to the sacrum was classified on midsagittal and midcoronal images (4 points per ring) by two observers. The ring apophysis maturation (RAM) was compared between different ages, sexes, and spinal levels. The RAM strongly correlated with age (R = 0.892, p < 0.001). Maturation differed in different regions of Citation: Costa, L.; de Reuver, S.; the spine and between sexes. High thoracic and low lumbar levels fused earlier in both groups, but, Kan, L.; Seevinck, P.; Kruyt, M.C.; around the peak of the growth spurt, in girls the mid-thoracic levels were less mature than in boys, Schlosser, T.P.C.; Castelein, R.M. which may have implications for the development of scoliosis. Ossification and Fusion of the Vertebral Ring Apophysis as an Keywords: ring apophysis; maturation; ossification; fusion; scoliosis Important Part of Spinal Maturation. J. Clin. Med. 2021, 10, 3217. https:// doi.org/10.3390/jcm10153217 1. Introduction Academic Editor: Theodoros The majority of pediatric spinal deformities develop during puberty when the body B. Grivas weight and dimensions increase rapidly, as the skeleton matures into its adult form. Recent studies have demonstrated the significant contribution of the intervertebral Received: 7 July 2021 discs to the deformation of the spine in scoliosis [1–3]. For undisturbed and harmonious Accepted: 20 July 2021 Published: 21 July 2021 spinal development, rapidly increasing loads during the growth spurt require adequate maturation of the spine’s stabilizers, of which the disc is an essential component [4]. Skeletal Publisher’s Note: MDPI stays neutral maturity is traditionally assessed on X-rays of the iliac crest, the hand, and wrists, or other with regard to jurisdictional claims in growth cartilages remote from the spine. The most used classifications are the Risser grade published maps and institutional affil- based on ossification and fusion of the iliac apophysis and the Sanders simplified skeletal iations. maturity scoring system, based on the maturation of the hand epiphyses [5,6]. Another classification is the Proximal Humerus Ossification System (PHOS) [7]. This classification is a five-stage system that uses the proximal humeral physis in assessing skeletal maturity. These skeletal maturation scoring systems correlate with the Peak Height Velocity (PHV) during pubertal growth and the curve acceleration phase in scoliosis, however, they do not Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. necessarily assess the maturation of different regions of the spine itself [6,8–10]. This article is an open access article After the formation of the three primary ossification centers for each vertebra (one for distributed under the terms and the body and two for the vertebral arch), the maturation of the spine continues with the conditions of the Creative Commons closure of the neurocentral synchondroses from age 4–8 [11]. The secondary ossification Attribution (CC BY) license (https:// centers are the ring apophyses and the tips of the transverse and spinous processes [12]. The creativecommons.org/licenses/by/ ring apophyses are not inside the epiphyseal plate and are not involved in the longitudinal 4.0/). growth of the spine [13]. During growth, they encircle the inferior and superior surfaces J. Clin. Med. 2021, 10, 3217. https://doi.org/10.3390/jcm10153217 https://www.mdpi.com/journal/jcm J. Clin. Med. 2021, 10, 3217 2 of 11 J. Clin. Med. 2021, 10, 3217 2 of 10 processes [12]. The ring apophyses are not inside the epiphyseal plate and are not involved in the longitudinal growth of the spine [13]. During growth, they encircle the ofinferior the vertebral and superior bodies. surfaces The outermost of the vertebral fibers of bodies. the annulus The outermost fibrosus, the fibers Sharpey’s of the annulus fibers, insertfibrosus, into thethe ringSharpey’s apophysis fibers, and insert thus anchor into the the intervertebralring apophysis disc and to thethus two anchor adjacent the vertebraeintervertebral (Figure disc1)[ to14 the–18 ].two During adjacent skeletal vertebrae maturation, (Figure these 1) [1 initially4–18]. During cartilaginous skeletal insertionsmaturation, of thethese disc initially ossify cartilaginous and ultimately insertions fuse to the of the vertebral disc ossify bodies and [19 ultimately]. This process fuse to hasthe important vertebral implicationsbodies [19]. forThis the process mechanical has stabilityimportant of theimplications disc-vertebral for the body mechanical complex atstability a time when of the spinal disc- loadingvertebral increases body complex rapidly, butat a very time little when is known spinal about loading its differentincreases phasesrapidly, during but very growth little [20 is ,known21]. about its different phases during growth [20,21]. FigureFigure 1. 1.( a()a) A A view view of of the the ossified ossified rings rings and and the the start start of of the the fusion fusion (red (red circles) circles) to to the the vertebral vertebral body; body; (b ()b schematic) schematic anatomicalanatomical view view of of the the IVD IVD andand thethe attachmentattachment ofof thethe Sharpey’sSharpey’s fibersfibers to cartilage tissue. A: A: cartilaginous cartilaginous endplate. endplate. B: B:Nucleus Nucleus pulposus. pulposus. C: C: Anulus Anulus fibrosus. fibrosus. 2.2. Materials Materials and and Methods Methods 2.1.2.1. Study Study Population Population AfterAfter a waivera waiver from from the ethicalthe ethical review review board (ERB)board for(ERB) formal for review formal of review this retrospec- of this tiveretrospective study, pre-existing study, pre high-resolution-existing high- Computedresolution TomographyComputed Tomography (CT) scans of(CT) the scans thorax of and/orthe thorax abdomen and/or acquired abdomen from acquired a tertiary from pediatric a tertiary hospital pediatric for hospital indications for indications not related tonot thisrelat studyed to (e.g., this trauma study screening,(e.g., trauma pulmonary screening, disease, pulmonary and gastro-enteric disease, and disorders) gastro-enteric were includeddisorders) from were our included local patient from archiving our local and patient communications archiving and system communications (PACS). Inclusion system criteria(PACS). were Inclusion patients criteria between were 6 andpatients 21 years between of age 6 and and 21 available years of high-resolution age and available images high- ofre thesolution spine images (slice thickness of the spine≤ 1 (slice mm and thickness slice interval ≤ 1 mm≤ and1.5 slice mm). interval The ages ≤ 1.5 of 6mm). and The 21 wereages chosenof 6 and based 21 were on chosen previous based studies on previous by Woo studies et al. andby Woo Uys et et al. al. and [13 ,Uys19]. et Exclusion al. [13,19]. criteriaExclusion were thecriteria presence were of spinalthe presence pathology, of bone spinal disorders pathology, (e.g., Scheuermann’s bone disorders disease), (e.g., syndromesScheuermann’s associated disease), with syndromes growth disorders, associated growth with hormone growth disorders, treatment, growth and insufficient hormone CT-scantreatment, quality and includinginsufficient movement CT-scan quality artifacts. including According movement to all available artifacts. information,According to subjectsall available represented information, healthy subjects adolescents. represented A minimum healthy of 10adolescents. subjects per A ageminimum cohort wasof 10 included.subjects Age,per age sex, cohort Risser grade,was included. and proximal Age, humeralsex, Risser ossification grade, and system proximal (PHOS) humeral were collectedossification on thesystem coronal (PHOS) survey were scans. collected on the coronal survey scans. 2.2. CT-Scan Analysis 2.2. CT-Scan Analysis The included CT scans were analyzed independently by two trained observers, who The included CT scans were analyzed independently by two trained observers, who scored each vertebra separately blinded from each other. Multiplanar images of the exact scored each vertebra separately blinded from each other. Multiplanar images of the exact mid-sagittal and mid-coronal plane of each individual vertebra were reconstructed, using mid-sagittal and mid-coronal plane of each individual