MR-based proton density fat fraction (PDFF) of the vertebral bone marrow differentiates between patients with and without osteoporotic vertebral fractures.
bone marrow
magnetic resonance imaging
osteoporosis
spine
Journal
Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA
ISSN: 1433-2965
Titre abrégé: Osteoporos Int
Pays: England
ID NLM: 9100105
Informations de publication
Date de publication:
Feb 2022
Feb 2022
Historique:
received:
01
09
2020
accepted:
03
09
2021
pubmed:
20
9
2021
medline:
8
2
2022
entrez:
19
9
2021
Statut:
ppublish
Résumé
The bone marrow proton density fat fraction (PDFF) assessed with MRI enables the differentiation between osteoporotic/osteopenic patients with and without vertebral fractures. Therefore, PDFF may be a potentially useful biomarker for bone fragility assessment. To evaluate whether magnetic resonance imaging (MRI)-based proton density fat fraction (PDFF) of vertebral bone marrow can differentiate between osteoporotic/osteopenic patients with and without vertebral fractures. Of the 52 study patients, 32 presented with vertebral fractures of the lumbar spine (66.4 ± 14.4 years, 62.5% women; acute low-energy osteoporotic/osteopenic vertebral fractures, N = 25; acute high-energy traumatic vertebral fractures, N = 7). These patients were frequency matched for age and sex to patients without vertebral fractures (N = 20, 69.3 ± 10.1 years, 70.0% women). Trabecular bone mineral density (BMD) values were derived from quantitative computed tomography. Chemical shift encoding-based water-fat MRI of the lumbar spine was performed, and PDFF maps were calculated. Associations between fracture status and PDFF were assessed using multivariable linear regression models. Over all patients, mean PDFF and trabecular BMD correlated significantly (r = - 0.51, P < 0.001). In the osteoporotic/osteopenic group, those patients with osteoporotic/osteopenic fractures had a significantly higher PDFF than those without osteoporotic fractures after adjusting for age, sex, weight, height, and trabecular BMD (adjusted mean difference [95% confidence interval], 20.8% [10.4%, 30.7%]; P < 0.001), although trabecular BMD values showed no significant difference between the subgroups (P = 0.63). For the differentiation of patients with and without vertebral fractures in the osteoporotic/osteopenic subgroup using mean PDFF, an area under the receiver operating characteristic (ROC) curve (AUC) of 0.88 (P = 0.006) was assessed. When evaluating all patients with vertebral fractures, those with high-energy traumatic fractures had a significantly lower PDFF than those with low-energy osteoporotic/osteopenic vertebral fractures (P < 0.001). MR-based PDFF enables the differentiation between osteoporotic/osteopenic patients with and without vertebral fractures, suggesting the use of PDFF as a potential biomarker for bone fragility.
Identifiants
pubmed: 34537863
doi: 10.1007/s00198-021-06147-3
pii: 10.1007/s00198-021-06147-3
pmc: PMC8813693
doi:
Substances chimiques
Protons
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
487-496Informations de copyright
© 2021. The Author(s).
Références
Kuhn JP, Hernando D, Meffert PJ et al (2013) Proton-density fat fraction and simultaneous R2* estimation as an MRI tool for assessment of osteoporosis. Eur Radiol 23:3432–3439
pubmed: 23812246
pmcid: 4245295
Sanfelix-Gimeno G, Sanfelix-Genoves J, Hurtado I, Reig-Molla B, Peiro S (2013) Vertebral fracture risk factors in postmenopausal women over 50 in Valencia Spain. A population-based cross-sectional study. Bone 52:393–399
pubmed: 23103928
Nazrun AS, Tzar MN, Mokhtar SA, Mohamed IN (2014) A systematic review of the outcomes of osteoporotic fracture patients after hospital discharge: morbidity, subsequent fractures, and mortality. Ther Clin Risk Manag 10:937–948
pubmed: 25429224
pmcid: 4242696
Link TM, Kazakia G (2020) Update on imaging-based measurement of bone mineral density and quality. Curr Rheumatol Rep 22:13
pubmed: 32270332
pmcid: 7875476
Link TM (2012) Osteoporosis imaging: state of the art and advanced imaging. Radiology 263:3–17
pubmed: 22438439
pmcid: 3309802
Fazeli PK, Horowitz MC, MacDougald OA et al (2013) Marrow fat and bone–new perspectives. J Clin Endocrinol Metab 98:935–945
pubmed: 23393168
pmcid: 3590487
Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35–43
pubmed: 16932650
Zhao LJ, Jiang H, Papasian CJ et al (2008) Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. J Bone Miner Res 23:17–29
pubmed: 17784844
Dieckmeyer M, Ruschke S, Cordes C et al (2015) The need for T(2) correction on MRS-based vertebral bone marrow fat quantification: implications for bone marrow fat fraction age dependence. NMR Biomed 28:432–439
pubmed: 25683154
Karampinos DC, Melkus G, Baum T, Bauer JS, Rummeny EJ, Krug R (2014) Bone marrow fat quantification in the presence of trabecular bone: initial comparison between water-fat imaging and single-voxel MRS. Magn Reson Med 71:1158–1165
pubmed: 23657998
pmcid: 3759615
Cordes C, Baum T, Dieckmeyer M et al (2016) MR-based assessment of bone marrow fat in osteoporosis, diabetes, and obesity. Front Endocrinol (Lausanne) 7:74
Karampinos DC, Ruschke S, Dieckmeyer M et al (2018) Quantitative MRI and spectroscopy of bone marrow. J Magn Reson Imaging 47:332–353
pubmed: 28570033
Li GW, Xu Z, Chen QW et al (2014) Quantitative evaluation of vertebral marrow adipose tissue in postmenopausal female using MRI chemical shift-based water-fat separation. Clin Radiol 69:254–262
pubmed: 24286935
Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M (2001) Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology 2:165–171
pubmed: 11708718
Schmeel FC, Luetkens JA, Wagenhauser PJ et al (2018) Proton density fat fraction (PDFF) MRI for differentiation of benign and malignant vertebral lesions. Eur Radiol 28:2397–2405
pubmed: 29313118
Kim DH, Yoo HJ, Hong SH, Choi JY, Chae HD, Chung BM (2017) Differentiation of acute osteoporotic and malignant vertebral fractures by quantification of fat fraction with a Dixon MRI sequence. AJR Am J Roentgenol 209:1331–1339
pubmed: 28858543
Patsch JM, Li X, Baum T et al (2013) Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J Bone Miner Res 28:1721–1728
pubmed: 23558967
Schwartz AV, Sigurdsson S, Hue TF et al (2013) Vertebral bone marrow fat associated with lower trabecular BMD and prevalent vertebral fracture in older adults. J Clin Endocrinol Metab 98:2294–2300
pubmed: 23553860
pmcid: 3667265
Regis-Arnaud A, Guiu B, Walker PM, Krause D, Ricolfi F, Ben Salem D (2011) Bone marrow fat quantification of osteoporotic vertebral compression fractures: comparison of multi-voxel proton MR spectroscopy and chemical-shift gradient-echo MR imaging. Acta Radiol 52:1032–1036
pubmed: 21948596
Roski F, Hammel J, Mei K et al (2019) Bone mineral density measurements derived from dual-layer spectral CT enable opportunistic screening for osteoporosis. Eur Radiol 29:6355–6363
pubmed: 31115622
pmcid: 6795615
Loffler MT, Sollmann N, Mei K et al (2020) X-ray-based quantitative osteoporosis imaging at the spine. Osteoporos Int 31:233–250
pubmed: 31728606
Loffler MT, Jacob A, Valentinitsch A et al (2019) Improved prediction of incident vertebral fractures using opportunistic QCT compared to DXA. Eur Radiol 29:4980–4989
pubmed: 30790025
pmcid: 6682570
Engelke K, Adams JE, Armbrecht G et al (2008) Clinical use of quantitative computed tomography and peripheral quantitative computed tomography in the management of osteoporosis in adults: the 2007 ISCD Official Positions. J Clin Densitom 11:123–162
pubmed: 18442757
ACR (2013) ACR–SPR–SSR practice parameter for the performance of quantitative computed tomography (QCT) bone densitometry The American College of Radiology. https://www.acr.org/-/media/ACR/Files/Practice-Parameters/qct.pdf . Accessed 17 Dec 2020
Ruschke S, Eggers H, Kooijman H et al (2017) Correction of phase errors in quantitative water-fat imaging using a monopolar time-interleaved multi-echo gradient echo sequence. Magn Reson Med 78:984–996
pubmed: 27797100
Karampinos DC, Yu H, Shimakawa A, Link TM, Majumdar S (2011) T(1)-corrected fat quantification using chemical shift-based water/fat separation: application to skeletal muscle. Magn Reson Med 66:1312–1326
pubmed: 21452279
pmcid: 3150641
Diefenbach MN, Liu C, Karampinos DC (2020) Generalized parameter estimation in multi-echo gradient-echo-based chemical species separation. Quant Imaging Med Surg 10:554–567
pubmed: 32269917
pmcid: 7136725
Ren J, Dimitrov I, Sherry AD, Malloy CR (2008) Composition of adipose tissue and marrow fat in humans by 1H NMR at 7 Tesla. J Lipid Res 49:2055–2062
pubmed: 18509197
pmcid: 2515528
Baum T, Rohrmeier A, Syvari J et al (2018) Anatomical variation of age-related changes in vertebral bone marrow composition using chemical shift encoding-based water-fat magnetic resonance imaging. Front Endocrinol (Lausanne) 9:141
Dieckmeyer M, Junker D, Ruschke S et al (2020) Vertebral bone marrow heterogeneity using texture analysis of chemical shift encoding-based MRI: variations in age, sex, and anatomical location. Front Endocrinol (Lausanne) 11:555931
Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8:1137–1148
pubmed: 8237484
Magerl F, Aebi M, Gertzbein SD, Harms J, Nazarian S (1994) A comprehensive classification of thoracic and lumbar injuries. Eur Spine J 3:184–201
pubmed: 7866834
Vaccaro AR, Oner C, Kepler CK et al (2013) AOSpine thoracolumbar spine injury classification system: fracture description, neurological status, and key modifiers. Spine 38:2028–2037
pubmed: 23970107
Hedderich DM, Maegerlein C, Baum T et al (2019) Differentiation of acute/subacute versus old vertebral fractures in multislice detector computed tomography: is magnetic resonance imaging always needed? World Neurosurgery 122:e676–e683
pubmed: 30385360
Reeder SB, Sirlin CB (2010) Quantification of liver fat with magnetic resonance imaging. Magn Reson Imaging Clin N Am 18(337–357):ix
Reeder SB, Hu HH, Sirlin CB (2012) Proton density fat-fraction: a standardized MR-based biomarker of tissue fat concentration. J Magn Reson Imaging 36:1011–1014
pubmed: 22777847
pmcid: 4779595
Yokoo T, Shiehmorteza M, Hamilton G et al (2011) Estimation of hepatic proton-density fat fraction by using MR imaging at 3.0 T. Radiology 258:749–759
pubmed: 21212366
pmcid: 3042639
Griffith JF, Yeung DK, Antonio GE et al (2006) Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation. Radiology 241:831–838
pubmed: 17053202
Li X, Kuo D, Schafer AL et al (2011) Quantification of vertebral bone marrow fat content using 3 Tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging 33:974–979
pubmed: 21448966
pmcid: 3072841
Yeung DK, Griffith JF, Antonio GE, Lee FK, Woo J, Leung PC (2005) Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study. J Magn Reson Imaging 22:279–285
pubmed: 16028245
Griffith JF, Yeung DK, Antonio GE et al (2005) Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology 236:945–951
pubmed: 16055699
Tang GY, Lv ZW, Tang RB et al (2010) Evaluation of MR spectroscopy and diffusion-weighted MRI in detecting bone marrow changes in postmenopausal women with osteoporosis. Clin Radiol 65:377–381
pubmed: 20380936
Li G, Xu Z, Gu H et al (2017) Comparison of chemical shift-encoded water-fat MRI and MR spectroscopy in quantification of marrow fat in postmenopausal females. J Magn Reson Imaging 45:66–73
pubmed: 27341545
Dunnill MS, Anderson JA, Whitehead R (1967) Quantitative histological studies on age changes in bone. J Pathol Bacteriol 94:275–291
pubmed: 6066476
Karampinos DC, Ruschke S, Gordijenko O et al (2015) Association of MRS-based vertebral bone marrow fat fraction with bone strength in a human in vitro model. J Osteoporos 2015:152349
pubmed: 25969766
pmcid: 4417596
Cheng X, Li K, Zhang Y et al (2020) The accurate relationship between spine bone density and bone marrow in humans. Bone 134:115312
pubmed: 32145459
Khoo BC, Brown K, Cann C et al (2009) Comparison of QCT-derived and DXA-derived areal bone mineral density and T scores. Osteoporos Int 20:1539–1545
pubmed: 19107384
Adams JE (2009) Quantitative computed tomography. Eur J Radiol 71:415–424
pubmed: 19682815
Guo Y, Chen Y, Zhang X et al (2019) Magnetic susceptibility and fat content in the lumbar spine of postmenopausal women with varying bone mineral density. J Magn Reson Imaging 49:1020–1028
pubmed: 30252983
Baum T, Yap SP, Karampinos DC et al (2012) 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 Magn Reson Imaging 35:117–124
pubmed: 22190287
Bredella MA, Daley SM, Kalra MK, Brown JK, Miller KK, Torriani M (2015) Marrow adipose tissue quantification of the lumbar spine by using dual-energy CT and single-voxel (1)H MR spectroscopy: a feasibility study. Radiology 277:230–235
pubmed: 25988401
Kuiper JW, van Kuijk C, Grashuis JL, Ederveen AG, Schutte HE (1996) Accuracy and the influence of marrow fat on quantitative CT and dual-energy X-ray absorptiometry measurements of the femoral neck in vitro. Osteoporos Int 6:25–30
pubmed: 8845596
Laval-Jeantet AM, Roger B, Bouysee S, Bergot C, Mazess RB (1986) Influence of vertebral fat content on quantitative CT density. Radiology 159:463–466
pubmed: 3961178
Loffler MT, Jacob A, Scharr A et al (2021) Automatic opportunistic osteoporosis screening in routine CT: improved prediction of patients with prevalent vertebral fractures compared to DXA. Eur Radiol 31:6069–6077
pubmed: 33507353
pmcid: 8270840
Loffler MT, Sollmann N, Burian E et al (2020) Opportunistic osteoporosis screening reveals low bone density in patients with screw loosening after lumbar semi-rigid instrumentation: a case-control study. Front Endocrinol (Lausanne) 11:552719
Loffler MT, Jacob A, Scharr A et al (2021) Automatic opportunistic osteoporosis screening in routine CT: improved prediction of patients with prevalent vertebral fractures compared to DXA. Eur Radiol. https://doi.org/10.1007/s00330-020-07655-2
doi: 10.1007/s00330-020-07655-2
pubmed: 33507353
pmcid: 8270840
Roski F, Hammel J, Mei K et al (2021) Opportunistic osteoporosis screening: contrast-enhanced dual-layer spectral CT provides accurate measurements of vertebral bone mineral density. Eur Radiol 31:3147–3155
pubmed: 33052464
Mookiah MRK, Rohrmeier A, Dieckmeyer M et al (2018) Feasibility of opportunistic osteoporosis screening in routine contrast-enhanced multi detector computed tomography (MDCT) using texture analysis. Osteoporos Int 29:825–835
pubmed: 29322221