Early screening and timely treatment can effectively reduce the morbidity and mortality of the osteoporotic fractures, and hence efficient and accurate non-invasive radiological method is crucial. Non-invasive imaging methods of radiology frequently encounter less resistance in the promotion of therapeutic activities than invasive procedures like bone biopsy and perfusion imaging. Although dual-energy X-ray absorption has been established as the primary diagnostic method for osteoporosis, its efficacy is relatively constrained due to various parameters, and it is challenging to accurately depict the true status of bone structure. In recent years, radiological techniques have developed rapidly. Computed tomography, magnetic resonance imaging, quantitative ultrasound and other imaging techniques have been widely used in the diagnosis of osteoporosis in the research and clinical practices, which provides more comprehensive and detailed information about bone mineral density and bone structure for early diagnosis, treatment design and prognosis monitoring. As clinic and computer science crosstalk closely, it will become possible for artificial intelligence to assist or even independently perform imaging analysis and disease screening in image data base. This article reviews the individual characteristics and latest research progress of the non-invasive radiological techniques for the osteoporosis.
Keywords：osteoporosis
;
bone mineral density
;
dual energy X-ray absorptiometry
;
computed tomography
;
magnetic resonance imaging
LIU Chenjun, YIN Bohao, SUN Hui, ZHANG Wei. Application of non-invasive methods of radiology to the osteoporosis. Journal of Shanghai Jiao Tong University (Medical Science)[J], 2023, 43(3): 385-390 doi:10.3969/j.issn.1674-8115.2023.03.016
骨质疏松症（osteoporosis，OP）是以骨量减少和骨结构退变为特征的全身代谢性疾病。随着中国老龄化加剧、OP发病率逐渐增高，如何敏感且高效地筛查和确诊OP成为亟待解决的难题，这不仅影响OP预防开展和治疗策略，还关乎OP及并发症的预测和预后评估。世界卫生组织推荐基于双能X射线吸收法（dual energy X-ray absorptiometry，DXA）测定骨密度（bone mineral density，BMD）。对于低能量或非外伤性骨折，在排除其他相关骨疾病后，即使骨密度不满足测定要求，也应诊断为OP。发生脆性骨折人群中的20%~30%DXA测量的BMD不满足OP的诊断条件仍发生脆性骨折［1］，由此可见DXA并不是骨强度的综合体现，需要新的技术手段和判断指标补充。侵入性影像学技术如显微计算机断层扫描技术和造影剂灌注成像往往难以被受试者接受［2］，而且不便应用于大规模筛查和OP长期监控。近年来非侵入性影像学技术的相关研究不断进展，故现对其在OP诊治中的应用研究进展进行综述。
1 影像学技术
1.1 双能X射线吸收法
DXA反映的是骨组织面积骨密度（area bone mineral density，aBMD），严格地说并不是真实的骨密度，易受所测区域骨体积大小影响而产生偏倚［3］。此外aBMD是感兴趣区所含骨量的综合反映，包含骨皮质和骨松质。测量区域周围的矿物质变化会造成DXA测量误差，如腰椎DXA容易受主动脉等大血管钙化、骨赘生成等造成aBMD增大，无法反映真实情况［4］。
随着DXA分辨率和后处理能力的提升，骨小梁分数（trabecular bone score，TBS）、骨应力指数（bone strain index，BSI）等参数通过分析DXA影像像素灰阶的分布与变化，可补充DXA对于骨小梁结构的评估［5-7］；3D-DXA技术则根据所得影像运用3D-2D算法等后处理模拟三维结构，得到体积骨密度（volumetric bone mineral density，vBMD）、皮质骨vBMD和皮质骨厚度等参数［8］。有研究提出3D-DXA还可以测量股骨近端屈曲比、横截面积、截面转动惯量等几何结构参数，以定量计算机断层扫描（quantitative computed tomography，QCT）为标准比较，发现截面结构参数相关系数r=0.86~0.96，且体积结构参数r=0.84~0.97，3D-DXA具有评估股骨骨强度的潜力［9］。但主要困难是非直接测量带来的偏倚和较长的后处理时间，其次是多样的机器和算法阻碍同类研究间的分析。需要强调的是，TBS、BSI以及3D-DXA并不是骨微结构的直接反映，只是根据DXA影像的分析，有待于更多研究验证。
The manuscript was drafted by LIU Chenjun and revised by ZHANG Wei, SUN Hui and YIN Bohao. All the authors have read the last version of paper and consented for submission.
利益冲突声明
所有作者声明不存在利益冲突。
All authors disclose no relevant conflict of interests.
WRIGHT N C, SAAG K G, DAWSON-HUGHES B, et al. The impact of the new National Bone Health Alliance (NBHA) diagnostic criteria on the prevalence of osteoporosis in the United States: supplementary presentation[J]. Osteoporos Int, 2017, 28(11): 3283-3284.
KIMMEL D B, VENNIN S, DESYATOVA A, et al. Bone architecture, bone material properties, and bone turnover in non-osteoporotic post-menopausal women with fragility fracture[J]. Osteoporos Int, 2022, 33(5): 1125-1136.
PADLINA I, GONZALEZ-RODRIGUEZ E, HANS D, et al. The lumbar spine age-related degenerative disease influences the BMD not the TBS: the Osteolaus cohort[J]. Osteoporos Int, 2017, 28(3): 909-915.
RAJAN R, CHERIAN K E, KAPOOR N, et al. Trabecular bone score-an emerging tool in the management of osteoporosis[J]. Indian J Endocrinol Metab, 2020, 24(3): 237-243.
MESSINA C, RINAUDO L, CESANA B M, et al. Prediction of osteoporotic fragility re-fracture with lumbar spine DXA-based derived bone strain index: a multicenter validation study[J]. Osteoporos Int, 2021, 32(1): 85-91.
HUMBERT L, MARTELLI Y, FONOLLÀ R, et al. 3D-DXA: assessing the femoral shape, the trabecular macrostructure and the cortex in 3D from DXA images[J]. IEEE Trans Med Imaging, 2017, 36(1): 27-39.
CLOTET J, MARTELLI Y, DI GREGORIO S, et al. Structural parameters of the proximal femur by 3-dimensional dual-energy X-ray absorptiometry software: comparison with quantitative computed tomography[J]. J Clin Densitom, 2018, 21(4): 550-562.
HE Q F, SUN H, SHU L Y, et al. Radiographic predictors for bone mineral loss: cortical thickness and index of the distal femur[J]. Bone Joint Res, 2018, 7(7): 468-475.
LIM H K, HA H I, PARK S Y, et al. Comparison of the diagnostic performance of CT Hounsfield unit histogram analysis and dual-energy X-ray absorptiometry in predicting osteoporosis of the femur[J]. Eur Radiol, 2019, 29(4): 1831-1840.
LI Y L, WONG K H, LAW M W M, et al. Opportunistic screening for osteoporosis in abdominal computed tomography for Chinese population[J]. Arch Osteoporos, 2018, 13(1): 76.
POOLE K E, TREECE G M, PEARSON R A, et al. Romosozumab enhances vertebral bone structure in women with low bone density[J]. J Bone Miner Res, 2022, 37(2): 256-264.
SU Y B, WANG L, LIU X Y, et al. Lack of periosteal apposition in the head and neck of femur after menopause in Chinese women with high risk for hip fractures—a cross-sectional study with QCT[J]. Bone, 2020, 139: 115545.
CHEN X G, WANG L, ZENG Q, et al. Chinese guideline for the diagnosis of osteoporosis with quantitative computed tomography(2018)[J]. Chin J Health Manage, 2019, 5(3): 195-200.
SCHULTE F A, CHRISTEN P, BADILATTI S D, et al. Virtual supersampling as post-processing step preserves the trabecular bone morphometry in human peripheral quantitative computed tomography scans[J]. PLoS One, 2019, 14(2): e0212280.
HANSEN S, SHANBHOGUE V, FOLKESTAD L, et al. Bone microarchitecture and estimated strength in 499 adult Danish women and men: a cross-sectional, population-based high-resolution peripheral quantitative computed tomographic study on peak bone structure[J]. Calcif Tissue Int, 2014, 94(3): 269-281.
SAMELSON E J, BROE K E, XU H F, et al. Cortical and trabecular bone microarchitecture as an independent predictor of incident fracture risk in older women and men in the Bone Microarchitecture International Consortium (BoMIC): a prospective study[J]. Lancet Diabetes Endocrinol, 2019, 7(1): 34-43.
ALVARENGA J C, CAPARBO V F, DOMICIANO D S, et al. Age-related reference data of bone microarchitecture, volumetric bone density, and bone strength parameters in a population of healthy Brazilian men: an HR-pQCT study[J]. Osteoporos Int, 2022, 33(6): 1309-1321.
RAMCHAND S K, DAVID N L, LEE H, et al. Effects of combination denosumab and high-dose teriparatide administration on bone microarchitecture and estimated strength: the DATA-HD HR-pQCT study[J]. J Bone Miner Res, 2021, 36(1): 41-51.
NILSSON A G, SUNDH D, JOHANSSON L, et al. Type 2 diabetes mellitus is associated with better bone microarchitecture but lower bone material strength and poorer physical function in elderly women: a population-based study[J]. J Bone Miner Res, 2017, 32(5): 1062-1071.
MANSKE S L, DAVISON E M, BURT L A, et al. The estimation of second-generation HR-pQCT from first-generation HR-pQCT using in vivo cross-calibration[J]. J Bone Miner Res, 2017, 32(7): 1514-1524.
SODICKSON A D, KERALIYA A, CZAKOWSKI B, et al. Dual energy CT in clinical routine: how it works and how it adds value[J]. Emerg Radiol, 2021, 28(1): 103-117.
ZHOU S W, ZHU L, YOU T, et al. In vivo quantification of bone mineral density of lumbar vertebrae using fast kVp switching dual-energy CT: correlation with quantitative computed tomography[J]. Quant Imaging Med Surg, 2021, 11(1): 341-350.
SHEN W, SCHERZER R, GANTZ M, et al. Relationship between MRI-measured bone marrow adipose tissue and hip and spine bone mineral density in African-American and Caucasian participants: the CARDIA study[J]. J Clin Endocrinol Metab, 2012, 97(4): 1337-1346.
LI J, CHEN X, LU L Y, et al. The relationship between bone marrow adipose tissue and bone metabolism in postmenopausal osteoporosis[J]. Cytokine Growth Factor Rev, 2020, 52: 88-98.
LIU Z H, ZHANG Y T, LIU Z, et al. Dual-energy computed tomography virtual noncalcium technique in diagnosing osteoporosis: correlation with quantitative computed tomography[J]. J Comput Assist Tomogr, 2021, 45(3): 452-457.
WICHMANN J L, BOOZ C, WESARG S, et al. Dual-energy CT-based phantomless in vivo three-dimensional bone mineral density assessment of the lumbar spine[J]. Radiology, 2014, 271(3): 778-784.
BOOZ C, HOFMANN P C, SEDLMAIR M, et al. Evaluation of bone mineral density of the lumbar spine using a novel phantomless dual-energy CT post-processing algorithm in comparison with dual-energy X-ray absorptiometry[J]. Eur Radiol Exp, 2017, 1(1): 11.
CHANG G, HONIG S, LIU Y X, et al. 7 Tesla MRI of bone microarchitecture discriminates between women without and with fragility fractures who do not differ by bone mineral density[J]. J Bone Miner Metab, 2015, 33(3): 285-293.
RAJAPAKSE C S, HOTCA A, NEWMAN B T, et al. Patient-specific hip fracture strength assessment with microstructural MR imaging-based finite element modeling[J]. Radiology, 2017, 283(3): 854-861.
RAJAPAKSE C S, FARID A R, KARGILIS D C, et al. MRI-based assessment of proximal femur strength compared to mechanical testing[J]. Bone, 2020, 133: 115227.
ZHANG L Y, WANG L, FU R S, et al. In vivo assessment of age- and loading configuration-related changes in multiscale mechanical behavior of the human proximal femur using MRI-based finite element analysis[J]. J Magn Reson Imaging, 2021, 53(3): 905-912.
JERBAN S, MA Y J, JANG H, et al. Water proton density in human cortical bone obtained from ultrashort echo time (UTE) MRI predicts bone microstructural properties[J]. Magn Reson Imaging, 2020, 67: 85-89.
BAUM T, YAP S P, KARAMPINOS D C, et al. Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine bone mineral density, and blood biomarkers in women with type 2 diabetes mellitus?[J]. J Magn Reson Imaging, 2012, 35(1): 117-124.
HE J, FANG H, LI X N. Vertebral bone marrow fat content in normal adults with varying bone densities at 3T magnetic resonance imaging[J]. Acta Radiol, 2019, 60(4): 509-515.
LI X J, SHET K, XU K P, et al. Unsaturation level decreased in bone marrow fat of postmenopausal women with low bone density using high resolution magic angle spinning (HRMAS) 1H NMR spectroscopy[J]. Bone, 2017, 105: 87-92.
WOODS G N, EWING S K, SCHAFER A L, et al. Saturated and unsaturated bone marrow lipids have distinct effects on bone density and fracture risk in older adults[J]. J Bone Miner Res, 2022, 37(4): 700-710.
GUO Y H, CHEN Y J, ZHANG X T, et al. Magnetic susceptibility and fat content in the lumbar spine of postmenopausal women with varying bone mineral density[J]. J Magn Reson Imaging, 2019, 49(4): 1020-1028.
MOMENI M, ASADZADEH M, MOWLA K, et al. Sensitivity and specificity assessment of DWI and ADC for the diagnosis of osteoporosis in postmenopausal patients[J]. Radiol med, 2020, 125(1): 68-74.
MOAYYERI A, ADAMS J E, ADLER R A, et al. Quantitative ultrasound of the heel and fracture risk assessment: an updated meta-analysis[J]. Osteoporos Int, 2012, 23(1): 143-153.
MCCLOSKEY E V, KANIS J A, ODÉN A, et al. Predictive ability of heel quantitative ultrasound for incident fractures: an individual-level meta-analysis[J]. Osteoporos Int, 2015, 26(7): 1979-1987.
LIU Z J, ZHANG C, MA C, et al. Automatic phantom-less QCT system with high precision of BMD measurement for osteoporosis screening: technique optimisation and clinical validation[J]. J Orthop Transl, 2022, 33: 24-30.
LI Y C, CHEN H H, LU H H S, et al. Can a deep-learning model for the automated detection of vertebral fractures approach the performance level of human subspecialists?[J]. Clin Orthop Relat Res, 2021, 479(7): 1598-1612.
FANG Y J, LI W, CHEN X J, et al. Opportunistic osteoporosis screening in multi-detector CT images using deep convolutional neural networks[J]. Eur Radiol, 2021, 31(4): 1831-1842.
... 骨质疏松症（osteoporosis，OP）是以骨量减少和骨结构退变为特征的全身代谢性疾病.随着中国老龄化加剧、OP发病率逐渐增高，如何敏感且高效地筛查和确诊OP成为亟待解决的难题，这不仅影响OP预防开展和治疗策略，还关乎OP及并发症的预测和预后评估.世界卫生组织推荐基于双能X射线吸收法（dual energy X-ray absorptiometry，DXA）测定骨密度（bone mineral density，BMD）.对于低能量或非外伤性骨折，在排除其他相关骨疾病后，即使骨密度不满足测定要求，也应诊断为OP.发生脆性骨折人群中的20%~30%DXA测量的BMD不满足OP的诊断条件仍发生脆性骨折［1］，由此可见DXA并不是骨强度的综合体现，需要新的技术手段和判断指标补充.侵入性影像学技术如显微计算机断层扫描技术和造影剂灌注成像往往难以被受试者接受［2］，而且不便应用于大规模筛查和OP长期监控.近年来非侵入性影像学技术的相关研究不断进展，故现对其在OP诊治中的应用研究进展进行综述. ...
1
... 骨质疏松症（osteoporosis，OP）是以骨量减少和骨结构退变为特征的全身代谢性疾病.随着中国老龄化加剧、OP发病率逐渐增高，如何敏感且高效地筛查和确诊OP成为亟待解决的难题，这不仅影响OP预防开展和治疗策略，还关乎OP及并发症的预测和预后评估.世界卫生组织推荐基于双能X射线吸收法（dual energy X-ray absorptiometry，DXA）测定骨密度（bone mineral density，BMD）.对于低能量或非外伤性骨折，在排除其他相关骨疾病后，即使骨密度不满足测定要求，也应诊断为OP.发生脆性骨折人群中的20%~30%DXA测量的BMD不满足OP的诊断条件仍发生脆性骨折［1］，由此可见DXA并不是骨强度的综合体现，需要新的技术手段和判断指标补充.侵入性影像学技术如显微计算机断层扫描技术和造影剂灌注成像往往难以被受试者接受［2］，而且不便应用于大规模筛查和OP长期监控.近年来非侵入性影像学技术的相关研究不断进展，故现对其在OP诊治中的应用研究进展进行综述. ...
1
... DXA反映的是骨组织面积骨密度（area bone mineral density，aBMD），严格地说并不是真实的骨密度，易受所测区域骨体积大小影响而产生偏倚［3］.此外aBMD是感兴趣区所含骨量的综合反映，包含骨皮质和骨松质.测量区域周围的矿物质变化会造成DXA测量误差，如腰椎DXA容易受主动脉等大血管钙化、骨赘生成等造成aBMD增大，无法反映真实情况［4］. ...
1
... DXA反映的是骨组织面积骨密度（area bone mineral density，aBMD），严格地说并不是真实的骨密度，易受所测区域骨体积大小影响而产生偏倚［3］.此外aBMD是感兴趣区所含骨量的综合反映，包含骨皮质和骨松质.测量区域周围的矿物质变化会造成DXA测量误差，如腰椎DXA容易受主动脉等大血管钙化、骨赘生成等造成aBMD增大，无法反映真实情况［4］. ...
1
... 随着DXA分辨率和后处理能力的提升，骨小梁分数（trabecular bone score，TBS）、骨应力指数（bone strain index，BSI）等参数通过分析DXA影像像素灰阶的分布与变化，可补充DXA对于骨小梁结构的评估［5-7］；3D-DXA技术则根据所得影像运用3D-2D算法等后处理模拟三维结构，得到体积骨密度（volumetric bone mineral density，vBMD）、皮质骨vBMD和皮质骨厚度等参数［8］.有研究提出3D-DXA还可以测量股骨近端屈曲比、横截面积、截面转动惯量等几何结构参数，以定量计算机断层扫描（quantitative computed tomography，QCT）为标准比较，发现截面结构参数相关系数r=0.86~0.96，且体积结构参数r=0.84~0.97，3D-DXA具有评估股骨骨强度的潜力［9］.但主要困难是非直接测量带来的偏倚和较长的后处理时间，其次是多样的机器和算法阻碍同类研究间的分析.需要强调的是，TBS、BSI以及3D-DXA并不是骨微结构的直接反映，只是根据DXA影像的分析，有待于更多研究验证. ...
0
1
... 随着DXA分辨率和后处理能力的提升，骨小梁分数（trabecular bone score，TBS）、骨应力指数（bone strain index，BSI）等参数通过分析DXA影像像素灰阶的分布与变化，可补充DXA对于骨小梁结构的评估［5-7］；3D-DXA技术则根据所得影像运用3D-2D算法等后处理模拟三维结构，得到体积骨密度（volumetric bone mineral density，vBMD）、皮质骨vBMD和皮质骨厚度等参数［8］.有研究提出3D-DXA还可以测量股骨近端屈曲比、横截面积、截面转动惯量等几何结构参数，以定量计算机断层扫描（quantitative computed tomography，QCT）为标准比较，发现截面结构参数相关系数r=0.86~0.96，且体积结构参数r=0.84~0.97，3D-DXA具有评估股骨骨强度的潜力［9］.但主要困难是非直接测量带来的偏倚和较长的后处理时间，其次是多样的机器和算法阻碍同类研究间的分析.需要强调的是，TBS、BSI以及3D-DXA并不是骨微结构的直接反映，只是根据DXA影像的分析，有待于更多研究验证. ...
1
... 随着DXA分辨率和后处理能力的提升，骨小梁分数（trabecular bone score，TBS）、骨应力指数（bone strain index，BSI）等参数通过分析DXA影像像素灰阶的分布与变化，可补充DXA对于骨小梁结构的评估［5-7］；3D-DXA技术则根据所得影像运用3D-2D算法等后处理模拟三维结构，得到体积骨密度（volumetric bone mineral density，vBMD）、皮质骨vBMD和皮质骨厚度等参数［8］.有研究提出3D-DXA还可以测量股骨近端屈曲比、横截面积、截面转动惯量等几何结构参数，以定量计算机断层扫描（quantitative computed tomography，QCT）为标准比较，发现截面结构参数相关系数r=0.86~0.96，且体积结构参数r=0.84~0.97，3D-DXA具有评估股骨骨强度的潜力［9］.但主要困难是非直接测量带来的偏倚和较长的后处理时间，其次是多样的机器和算法阻碍同类研究间的分析.需要强调的是，TBS、BSI以及3D-DXA并不是骨微结构的直接反映，只是根据DXA影像的分析，有待于更多研究验证. ...
1
... 随着DXA分辨率和后处理能力的提升，骨小梁分数（trabecular bone score，TBS）、骨应力指数（bone strain index，BSI）等参数通过分析DXA影像像素灰阶的分布与变化，可补充DXA对于骨小梁结构的评估［5-7］；3D-DXA技术则根据所得影像运用3D-2D算法等后处理模拟三维结构，得到体积骨密度（volumetric bone mineral density，vBMD）、皮质骨vBMD和皮质骨厚度等参数［8］.有研究提出3D-DXA还可以测量股骨近端屈曲比、横截面积、截面转动惯量等几何结构参数，以定量计算机断层扫描（quantitative computed tomography，QCT）为标准比较，发现截面结构参数相关系数r=0.86~0.96，且体积结构参数r=0.84~0.97，3D-DXA具有评估股骨骨强度的潜力［9］.但主要困难是非直接测量带来的偏倚和较长的后处理时间，其次是多样的机器和算法阻碍同类研究间的分析.需要强调的是，TBS、BSI以及3D-DXA并不是骨微结构的直接反映，只是根据DXA影像的分析，有待于更多研究验证. ...
