Trabecular bone micro-architecture and bone mineral density in adolescent idiopathic and congenital scoliosis
2009; Wiley; Volume: 1; Issue: 1 Linguagem: Inglês
10.1111/j.2757-7861.2008.00014.x
ISSN1757-7861
AutoresFeng Zhu, Yong Qiu, Hiu Yan Yeung, Kwong Man Lee, Jack C. Y. Cheng,
Tópico(s)Connective tissue disorders research
ResumoOrthopaedic SurgeryVolume 1, Issue 1 p. 78-83 Open Access Trabecular bone micro-architecture and bone mineral density in adolescent idiopathic and congenital scoliosis Feng Zhu MD, Feng Zhu MD Department of Spinal Surgery, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China,Search for more papers by this authorYong Qiu MD, Yong Qiu MD Department of Spinal Surgery, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China,Search for more papers by this authorHiu Yan Yeung MPhil, Hiu Yan Yeung MPhil Department of Orthopaedics and Traumatology andSearch for more papers by this authorKwong Man Lee PhD, Kwong Man Lee PhD Lee Hysan Clinical Research Laboratories, The Chinese University of Hong Kong, ChinaSearch for more papers by this authorChun-yiu Jack Cheng MD, Chun-yiu Jack Cheng MD Department of Orthopaedics and Traumatology andSearch for more papers by this author Feng Zhu MD, Feng Zhu MD Department of Spinal Surgery, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China,Search for more papers by this authorYong Qiu MD, Yong Qiu MD Department of Spinal Surgery, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China,Search for more papers by this authorHiu Yan Yeung MPhil, Hiu Yan Yeung MPhil Department of Orthopaedics and Traumatology andSearch for more papers by this authorKwong Man Lee PhD, Kwong Man Lee PhD Lee Hysan Clinical Research Laboratories, The Chinese University of Hong Kong, ChinaSearch for more papers by this authorChun-yiu Jack Cheng MD, Chun-yiu Jack Cheng MD Department of Orthopaedics and Traumatology andSearch for more papers by this author First published: 29 January 2009 https://doi.org/10.1111/j.1757-7861.2008.00014.xCitations: 13 Feng Zhu, MD, Department of Spinal Surgery, Drum Tower Hospital of Nanjing University Medical School, Nanjing, China 210008 Tel: 0086-25-83105121; Fax: 0086-25-83105121; Email: cnspine@hotmail.com AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Objective: To investigate the microstructure of trabecular bone in adolescent idiopathic scoliosis (AIS) and age-matched congenital scoliosis (CS), and to evaluate the bone mineral status of CS patients compared with normal controls and AIS patients. Methods: This study included 15 AIS and 16 CS female patients and 35 healthy female adolescents. Corrective surgery was indicated for the AIS and CS patients, from whom iliac crest biopsies were collected during autograft harvesting, and scanned by micro-computer tomography. Bone mineral status was assessed at the lumbar and hip areas in every patient by dual energy X-ray absorptiometry (DEXA). Results: Significantly lower lumbar and femoral neck bone mineral density (BMD) was found in AIS patient compared with normal controls. All BMD and bone mineral content (BMC) parameters were significantly lower in CS patients compared with age-matched normal controls. Under DEXA assessment significant associations between bone volume/tissue volume (BV/TV) and BMD values were observed. In the 3D model, BV/TV was significantly higher in AIS (19.9% ± 3.4%) than in CS (13.3% ± 3.0%, P < 0.05). Significant differences between AIS and CS were also found in trabecular thickness (Tb.Th) and bone surface/bone volume (BS/BV) (155.5 ± 54.9 µm vs. 108.1 ± 17.4 µm and 16.4% ± 3.3% vs. 22.0% ± 3.4% respectively, P < 0.05 in both). Conclusion: Lower bone mineral status and weak trabecular bone structure observed in AIS and CS justify further investigation of the bone mineral status in scoliosis of various etiologies. Introduction Based on dual energy X-ray absorptiometry (DEXA) or peripheral quantitative computed tomography (pQCT) measurements, generalized osteopenia in adolescent idiopathic scoliosis (AIS) has been reported in previous studies1, 2. However, in AIS the structural properties of trabecular bone remain unexplored. Besides comprehensive and systemic study of bone mineral density (BMD) in AIS, few studies cover the bone mineral status in scoliosis of other etiology. Congenital scoliosis (CS), the second most common etiology for scoliosis, results from disruption of normal vertebral development. But the etiology of CS needs further elucidation and the bone mineral status in CS is not clear. It is well known that the mechanical strength of bone is closely related to the bone mineral density (BMD)1-3. The biomechanical properties of bone include both material and structural properties4-6. Therefore, in addition to BMD, the micro-architecture of trabecular bone is another critical mechanical property of bone. Traditionally, histomorphometry measures trabecular morphometry from sections, and is based on two dimensions (2D). The third dimension may be achieved according to the concept of stereology as described by Parfitt et al.7. By converting serial 2D data from histomorphometry into three dimensions (3D), they used conventional stereology to measure (3D) parameters like bone fraction or trabecular bone number. Not until 1989 was a new modality for the direct examination of three-dimensional bone structure introduced by Feldkamp et al.8. It was based on high-resolution computed tomography (CT), and was a true three-dimensional reconstruction array with a typical resolution of 50 µm, which was more powerful than clinical CT. A large number of slices in each of three orthogonal directions greatly facilitate the study of structural anisotropy. Micro CT also becomes an essential technique to assess trabecular bone in 3D without any destructive sample processing. The aim of this study was to investigate the characteristics of bone mineral status, and the three dimensional structure of trabecular bone from the iliac crest in AIS and CS patients. Materials and methods Subject recruitment In the AIS group, there were 15 female patients with a mean age of 14.9 years (range, 12–19 years) and Cobb angle range 48°–104° (mean, 59°). The CS group consisted of 16 female patients aged 13–18 years with a mean age of 14.6 years and Cobb 40°–125° (mean, 60.6°). A normal control group consisted of 35 female adolescents with a mean age of 14.6 (range, 13–16 years). The diagnoses of AIS and CS were based on standardized clinical examinations and radiological investigations. Patients with neuromuscular disease, endocrine disease, skeletal dysplasia, connective tissue abnormalities or mental retardation were excluded from the study. No accompanying lung function failure or other dysfunctions in renal, cardiovascular or other systems were found in the CS group. BMD measurement Pre-operative bone mineral status assessment was made in AIS, CS and control groups using DEXA (Norland XR-26 Mark II; Norland, Fort Atkinson, WI, USA). BMD and bone mineral content (BMC) were measured at the right femoral neck and L2-4 spine. BMC and bone area were measured, and BMD, in g/cm2, was calculated by dividing BMC by bone area. Bone biopsy Correction surgery was indicated for these patients, and iliac crest biopsies were obtained with a Bordier trephine (5–7 mm core diameter) from a site located 2 cm beneath and behind the posterior superior iliac crest during autograft harvesting. Biopsy consents were approved by the Clinical Research Ethical Committee of The Chinese University of Hong Kong. Informed consents were sought from all subjects and their parents. Bone specimens were fixed with 4% neutral formalin for 24 h, and then changed to 70% ethanol for Micro CT scanning. Micro CT scan Fan beam micro-computer tomography (µCT40, Scanco Medical AG, Bassersdorf, Switzerland) was used for micro-architectural evaluation of the iliac crest biopsies. During scanning, the specimens were held in an airtight cylindrical sample holder provided by the manufacturer of the machine and filled with 75% ethanol. The range of interests (ROI) was defined as 70% of the whole iliac crest biopsy (Fig. 1). The number of consecutively morphed slices for analysis ranged from 121–189 due to variation in the size of biopsy. The threshold was set at 173 to obtain the best coverage of all trabecular bone and, for evaluation, cortical bone was excluded manually. Both direct and indirect techniques were employed to assess the structural indices, according to the manufacturer's manual. Reconstructed 3D images at a resolution of 20 µm were achieved for morphometric analysis (Fig. 2). Figure 1Open in figure viewerPowerPoint The region of interest and morphing of trabecular bone. Figure 2Open in figure viewerPowerPoint 3D trabecular bone micro-architecture in AIS and CS. Primary indices consisted of bone surface (BS) area, bone volume (BV) and total volume (TV). The way to calculate the primary indices has been described previously9. Briefly, the BS is calculated by the method of Marching Cubes10, 11. As TV represent the volume of the whole examined sample, BV/TV and BS/TV are normalized indices which can be used to compare sample of different size. By actually measuring distances in the 3-D space, the indices of 3-D images are directly assessed. Trabecular thickness (Tb.Th) is the average thickness of all bone voxels. Trabecular separation (Tb.Sp) is the thickness of the marrow cavities. Trabecular number (Tb.N) is taken as the inverse of the mean distance between the mid-axes of the observed structure. The structure model index (SMI) represents an estimation of the plate-rod characteristics of the structure. Ideal flat plates have an SMI of 0, whereas ideal cylindrical rods have a SMI of 3. The 2D derived indices were from primary indices assuming a plate model and applying stereological techniques. For the plate model, Tb.Th = 2 BV/BS. Tb.Sp was regarded as the thickness of the marrow cavities and the Tb.Sp = 2 (marrow surface, MS)/(marrow volume, MV) = 2(TV-BV)/BS. Tb.N was the number of plates per unit length, that is Tb.N = 0.5 BS/TV. Statistical analysis Data were interpreted by mean and standard deviation. Independent sample Student's t-test was employed to compare the differences between AIS and CS in all indices derived from iliac crest analysis. These included BMD measured by DEXA and 2D and 3D trabecular structural variables measured by micro CT. Correlations between BMD and micro CT measurements were also evaluated. All statistics were performed using SPSS software (Ver.11.0, Chicago, IL, USA) and P < 0.05 was regarded as significant. Results BMD measurement Significant differences in lower lumbar and femoral neck BMD were found between AIS patients and age-matched normal controls (Table 1). Table 1. BMD and BMC comparison between AIS and CS Groups Lumbar spine BMD (g/cm2) Lumbar spine BMC (g) Femur neck BMD (g/cm2) Femur neck BMC (g) AIS (n = 15) 0.83 ± 0.13† 32.3 ± 7.5 0.75 ± 0.10† 2.25 ± 0.38 CS (n = 16) 0.75 ± 0.15 24.0 ± 8.0‡ 0.67 ± 0.12‡ 1.95 ± 0.40‡ Normal (n = 35) 0.92 ± 0.16§ 36.2 ± 7.8§ 0.84 ± 0.13§ 2.38 ± 0.42§ Data expressed as mean ± SD. †AIS vs. Normal P < 0.05.‡AIS vs. CS P < 0.05.§Normal vs. CS P < 0.05. AIS, adolescent idiopathic scoliosis; BMC, bone mineral content; BMD, bone mineral density; CS, congenital scoliosis. All BMD and BMC parameters were significantly lower in CS patients compared with age-matched normal controls (Table 1). Lumbar BMC, femoral neck BMD and BMC were significantly lower in CS than in AIS (32.3 ± 7.5 g vs. 24.0 ± 8.0 g, P = 0.005; 0.75 ± 0.10 g/cm2 vs. 0.67 ± 0.12 g/cm2, P = 0.004; 2.25 ± 0.38 vs. 1.95 ± 0.40, P = 0.048 respectively), other parameters showed no significant difference (Table 1). 2D morphometry The BV/TV value was significantly higher in AIS (18.9% ± 2.1%) than in CS (13.3% ± 9.12%, P < 0.05). The Tb.N was larger and Tb.Sp smaller in AIS than in CS, these differences were not significant. Significant differences between AIS and CS were observed in the parameters of Tb.Th and BS/BV which were 103.5 ± 0.3 µm vs. 79.1 ± 0.2 µm and 19.0% ± 10.6% vs. 26.6% ± 20.0% respectively (P < 0.05 for both, Table 2). Table 2. 2D Histomorphometry by micro CT AIS vs. CS Groups BV/TV (%) TbN (1/mm) TbTh (µm) TbSp (µm) BS/BV (%) BS/TV AIS 18.9 ± 4.5 1.9 ± 0.4 103.5 ± 19.8 479.3 ± 120.4 19.0 ± 4.4 3.7 ± 0.8 CS 13.3 ± 3.0† 1.7 ± 0.3 79.0 ± 1.7† 537.0 ± 111.9 26.6 ± 4.5† 3.4 ± 0.6 Data expressed as mean ± SD. †AIS vs. CS P < 0.05. AIS, adolescent idiopathic scoliosis; BS/BV, bone surface/bone volume; BS/TV, bone surface/bone volume; BV/TV, bone volume/tissue volume; CS, congenital scoliosis; TbN, trabecular number; TbSp, trabecular separation; TbTh, trabecular thickness. 3D morphometry Significant differences were found in the parameters of BV/TV and Tb.Th with AIS having higher values than CS (19.9% ± 3.4% vs. 13.3% ± 3.0% and 155.5 ± 54.9 µm vs. 108.1 ± 17.4 µm, P < 0.05). The indices of BS/BV were significantly lower in AIS than in CS (16.4% ± 3.3% vs. 22.0% ± 3.4%, P < 0.05). The parameters of connectivity density (Conn.D) and Tb.N were higher in AIS compared with CS but these differences were not significant Table 3, Fig. 2). Table 3. 3D Histomorphometry by micro CT AIS vs. CS Groups BV/TV (%) ConnD SMI TbN (1/mm) TbTh (µm) TbSp (µm) BS/BV (%) AIS 19.9 ± 3.4 8.36 ± 3.93 1.50 ± 0.37 1.81 ± 0.31 156.0 ± 54.9 551.8 ± 12.6 16.4 ± 3.3 CS 13.3 ± 3.0† 8.13 ± 2.44 1.81 ± 0.34 1.77 ± 0.25 108.1 ± 17.4† 563.7 ± 9.5 22.0 ± 3.4† Data expressed as mean ± SD. †AIS vs. CS P < 0.05. AIS, adolescent idiopathic scoliosis; BS/BV, bone surface/bone volume; BV/TV, bone volume/tissue volume; ConnD, connectivity density; CS, congenital scoliosis; SMI, structure model index; TbSp, trabecular separation; TbTh, trabecular thickness. In the AIS and CS groups, the 3D model BV/TV correlated well with all the BMD and BMC parameters, while other Micro-CT indices did not correlate well (Table 4). Table 4. Correlation between micro CT Parameter and BMD & BMC Micro CT parameters AIS CS LSBMD LSBMC FNBMD FNBMC LSBMD LSBMC FNBMD FNBMC BV/TV 0.830* 0.944* 0.699* 0.665* 0.937* 0.783* 0.616* 0.570* TbN 0.344 0.373 0.108 0.413 0.375 0.515* 0.407 0.064 TbTh 0.115 0.185 0.260 0.035 0.654* 0.396 0.453 0.602* TbSp −0.266 −0.265 −0.055 −0.362 −0.320 −0.501* −0.411 −0.018 BS/BV −0.230 −0.319 −0.366 −0.098 −0.630* −0.401 −0.311 −0.631* * P < 0.05. AIS, adolescent idiopathic scoliosis; BMC, bone mineral content; BMD, bone mineral density; BS/BV, bone surface/bone volume; BV/TV, bone volume/tissue volume; CS, congenital scoliosis; FN, femoral neck; LS, lumbar spine; TbN, trabecular number; TbSp, trabecular separation; TbTh, trabecular thickness. Discussion Systemic lower BMD has been reported in AIS12-15. Cook et al. was the first team to evaluate bone density of scoliotic subjects aged 9 to 20 years, and they found significantly lower BMD of the lumbar spine and proximal hip than in age-matched control subjects. Our previous studies have also demonstrated that AIS girls have persistently lower BMD than controls on longitudinal follow-up, and lower histomorphometric parameters in a 2D histological study13-15. But the bone mineral status in CS, another large cohort of scoliosis, has not been reported so far. Consistent with our previous study, 15 AIS patients in the current study showed lower BMD compared with age-matched normal controls. But what made the story more meaningful was that even lower BMD and BMC were found in the CS group compared with the normal and AIS groups. Significant differences between CS and AIS groups were observed in the parameters of lumbar BMC, femoral neck BMD and BMC. The similar lumbar BMD but lower BMC can only be explained by the smaller X-ray projection area of L2–4, which is caused by smaller vertebrae in CS. The reason for small vertebrae in CS needs further investigation. Significantly lower BMD and BMC parameters compared with the normal age-matched group further proves that the bone mineral status is abnormal in our CS group. Besides DEXA assessment, 3D trabecular bone architecture and structural properties were evaluated in the AIS and CS groups, which have not been investigated up to date. Micro CT as a novel imaging modality was designed to assess the structural properties of trabecular bone. The conventional approach to histomorphologic measurements requires embedding, sectioning and image analysis, which is really time-consuming. Another limitation of the conventional method is that it is a destructive procedure which prevents other assessment of the sample. The technique of Micro CT is totally a non-invasive means of assessment and provides high-resolution 3D images of trabecular bone structures6, 16. Micro CT study not only provides a quantitative analysis of the mineralized tissue of a biopsy, but is also a means to study the structural changes in trabecular bone in terms of morphology and 3D. Some previous studies have observed a correlation between Micro CT parameters and BMD parameters derived from DEXA or pQCT6, 17. In one study on a rat osteoporosis model, tibial BMD measured by DEXA significantly correlated with BV/TV and Tb N measured by Micro CT17. In another osteoporosis animal model using goats, volumetric bone mineral measured by pQCT significantly correlated with architectural parameters measured by Micro CT6. Our current study found the BV/TV significantly correlated with all BMD parameters detected by DEXA machine, while this was not the case for other Micro CT parameters. The difference may be because BMD assessed by DEXA includes both cortical and trabecular bone, while trabecular bone density can be detected separately with the pQCT modality. So, trabecular bone properties of Tb.Th, Tb.N and Tb.Sp may not correlate well with BMD values from DEXA because of the interference of relatively thicker cortical bone in humans. In 2D morphometric evaluation three parameters: BV/TV, Tb.Th and BS/BV, were significantly different between AIS and CS. We interpret these differences to mean that trabecular bone from the iliac crest of CS patients contains less mineralized bone mass and thinner trabecular bone, and also that the trabecular bone is more plate-like compared to that of AIS patients. Glorieux et al. have reported the reference data for 2D histomorphometry in adolescents: they took iliac crest biopsies from 58 children and adolescents and investigated them by the traditional 2D histomorphometry method18. We compared our data with their age-matched (14.0–16.9 years of age) 2D data, and found that values were all significantly lower in our AIS and CS group. We note their group is ethnically Caucasian, but it is the only available trabecular morphometric reference. In 3D morphometric evaluation, significant differences were observed between the AIS and CS groups in regard to the parameters of BV/TV, Tb.Th and BS/BV. Firstly, CS patients have less bone mass in trabecular bone compared with AIS, which is consistent with the BMD and BMC findings. Thinner and less numerous trabeculae make the bone structure more vulnerable to external loading and jeopardize the mechanical stability of trabecular bone in CS patients. Less Conn.D means the inter-connection between the trabecular is decreased in CS patients. Large margins between trabecular bone also may be secondary to thinner TbTh, less TbN, and smaller ConnD. Large SMI imply the trabecular bone in CS is more plate-like, which means in terms of mechanical properties it is relatively weaker than rod-like, and more osteoporotic6, 17. The current study has further improved our knowledge about the micro-architectural characteristics of bone and bone mineral status in both AIS and CS patients. This is the first study to examine the bone quality and quantity in scoliosis of congenital etiology. BMD data compared with normal age-matched adolescents, and micro CT data compared with AIS patients, make the conclusions more solid. The significant differences found between AIS and normal in comparison with CS will draw more attention to the bone mineral status of the latter group in the future. CS is a lateral curvature of the spine resulting from disruption of normal vertebral development. A large variety of spinal anomalies can be observed in CS, all of which result from abnormal formation and segmentation of the vertebral precursors, called somites. Early occurrence of spinal deformity in CS patients may lead to less physical activity, suboptimal development of pulmonary function or even poorer nutritional condition. These may be responsible for the inferior condition of bone mineral in the CS group. Given well-proved general osteopenia in AIS patients, the lower BMD and weaker bone structural properties in CS may imply that a bone mineral problem is common to other etiologic categories of scoliosis. So, in scoliotic patients, more attention should be paid to bone mass status, which may relate to the progression, treatment and quality of life. Although Micro CT is an alternative approach to image and quantify trabecular bone in 3D, it has not yet provided information about bone dynamics such as mineral apposition rate after tetracycline labeling, or on bone formation and absorption. 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