Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography

Abstract

Introduction

The application of high-resolution peripheral quantitative computed tomography (HR-pQCT) to assess bone microarchitecture has grown rapidly since its introduction in 2005. As the use of HR-pQCT for clinical research continues to grow, there is an urgent need to form a consensus on imaging and analysis methodologies so that studies can be appropriately compared. In addition, with the recent introduction of the second-generation HrpQCT, which differs from the first-generation HR-pQCT in scan region, resolution, and morphological measurement techniques, there is a need for guidelines on appropriate reporting of results and considerations as the field adopts newer systems.

Methods

A joint working group between the International Osteoporosis Foundation, American Society of Bone and Mineral Research, and European Calcified Tissue Society convened in person and by teleconference over several years to produce the guidelines and recommendations presented in this document.

Results

An overview and discussion is provided for (1) standardized protocol for imaging distal radius and tibia sites using HR-pQCT, with the importance of quality control and operator training discussed; (2) standardized terminology and recommendations on reporting results; (3) factors influencing accuracy and precision error, with considerations for longitudinal and multi-center study designs; and finally (4) comparison between scanner generations and other high-resolution CT systems.

Conclusion

This article addresses the need for standardization of HR-pQCT imaging techniques and terminology, provides guidance on interpretation and reporting of results, and discusses unresolved issues in the field.

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References

  1. 1.

    Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515

    CAS  PubMed  Google Scholar 

  2. 2.

    Jobke B, Burghardt AJ, Muche B, Hahn M, Semler J, Amling M, Majumdar S, Busse B (2011) Trabecular reorganization in consecutive iliac crest biopsies when switching from bisphosphonate to strontium ranelate treatment. PLoS One 6:e23638

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Jobke B, Muche B, Burghardt AJ, Semler J, Link TM, Majumdar S (2011) Teriparatide in bisphosphonate-resistant osteoporosis: microarchitectural changes and clinical results after 6 and 18 months. Calcif Tissue Int 89:130–139

    CAS  PubMed  Google Scholar 

  4. 4.

    Burt LA, Bhatla JL, Hanley DA, Boyd SK (2017) Cortical porosity exhibits accelerated rate of change in peri- compared with post-menopausal women. Osteoporos Int 28:1423–1431

    CAS  PubMed  Google Scholar 

  5. 5.

    Burt LA, Liang Z, Sajobi TT, Hanley DA, Boyd SK (2016) Sex- and site-specific normative data curves for HR-pQCT. J Bone Miner Res 31:2041–2047

    PubMed  Google Scholar 

  6. 6.

    Burt LA, Macdonald HM, Hanley DA, Boyd SK (2014) Bone microarchitecture and strength of the radius and tibia in a reference population of young adults: an HR-pQCT study. Arch Osteoporos 9:183

    PubMed  Google Scholar 

  7. 7.

    Gabel L, Macdonald HM, McKay HA (2017) Sex differences and growth-related adaptations in bone microarchitecture, geometry, density, and strength from childhood to early adulthood: a mixed longitudinal HR-pQCT study. J Bone Miner Res 32:250–263

    PubMed  Google Scholar 

  8. 8.

    Gabel L, Macdonald HM, Nettlefold LA, McKay HA (2018) Sex-, ethnic-, and age-specific centile curves for pQCT- and HR-pQCT-derived measures of bone structure and strength in adolescents and young adults. J Bone Miner Res 33:987–1000

    CAS  PubMed  Google Scholar 

  9. 9.

    Hansen S, Shanbhogue V, Folkestad L, Nielsen MM, Brixen K (2014) 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. Calcif Tissue Int 94:269–281

    CAS  PubMed  Google Scholar 

  10. 10.

    Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK (2011) Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-based HR-pQCT study. J Bone Miner Res 26:50–62

    PubMed  Google Scholar 

  11. 11.

    Popp KL, Hughes JM, Martinez-Betancourt A, Scott M, Turkington V, Caksa S, Guerriere KI, Ackerman KE, Xu C, Unnikrishnan G, Reifman J, Bouxsein ML (2017) Bone mass, microarchitecture and strength are influenced by race/ethnicity in young adult men and women. Bone 103:200–208

    PubMed  Google Scholar 

  12. 12.

    Vilayphiou N, Boutroy S, Sornay-Rendu E, Van Rietbergen B, Chapurlat R (2016) Age-related changes in bone strength from HR-pQCT derived microarchitectural parameters with an emphasis on the role of cortical porosity. Bone 83:233–240

    PubMed  Google Scholar 

  13. 13.

    Milovanovic P, Adamu U, Simon MJ, Rolvien T, Djuric M, Amling M, Busse B (2015) Age- and sex-specific bone structure patterns portend bone fragility in radii and tibiae in relation to osteodensitometry: a high-resolution peripheral quantitative computed tomography study in 385 individuals. J Gerontol A Biol Sci Med Sci 70:1269–1275

    PubMed  Google Scholar 

  14. 14.

    Bacchetta J, Boutroy S, Vilayphiou N, Juillard L, Guebre-Egziabher F, Rognant N, Sornay-Rendu E, Szulc P, Laville M, Delmas PD, Fouque D, Chapurlat R (2010) Early impairment of trabecular microarchitecture assessed with HR-pQCT in patients with stage II-IV chronic kidney disease. J Bone Miner Res 25:849–857

    PubMed  Google Scholar 

  15. 15.

    Braun C, Bacchetta J, Braillon P, Chapurlat R, Drai J, Reix P (2017) Children and adolescents with cystic fibrosis display moderate bone microarchitecture abnormalities: data from high-resolution peripheral quantitative computed tomography. Osteoporos Int 28:3179–3188

    CAS  PubMed  Google Scholar 

  16. 16.

    Nour MA, Burt LA, Perry RJ, Stephure DK, Hanley DA, Boyd SK (2016) Impact of growth hormone on adult bone quality in turner syndrome: a HR-pQCT study. Calcif Tissue Int 98:49–59

    CAS  PubMed  Google Scholar 

  17. 17.

    Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu CT, Boyd SK, McLean RR, Broe KE, Kiel DP, Bouxsein ML (2018) Diabetes and deficits in cortical bone density, microarchitecture, and bone size: Framingham HR-pQCT Study. J Bone Miner Res 33:54–62

    PubMed  Google Scholar 

  18. 18.

    Boyd SK, Burt LA, Sevick LK, Hanley DA (2015) The relationship between serum 25(OH)D and bone density and microarchitecture as measured by HR-pQCT. Osteoporos Int 26:2375–2380

    CAS  PubMed  Google Scholar 

  19. 19.

    Burghardt AJ, Kazakia GJ, Sode M, de Papp AE, Link TM, Majumdar S (2010) A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res 25:2558–2571

    PubMed  PubMed Central  Google Scholar 

  20. 20.

    Tsai JN, Nishiyama KK, Lin D, Yuan A, Lee H, Bouxsein ML, Leder BZ (2017) Effects of denosumab and teriparatide transitions on bone microarchitecture and estimated strength: the DATA-Switch HR-pQCT study. J Bone Miner Res 32:2001–2009

    CAS  PubMed  Google Scholar 

  21. 21.

    Langsetmo L, Shikany JM, Burghardt AJ et al (2018) High dairy protein intake is associated with greater bone strength parameters at the distal radius and tibia in older men: a cross-sectional study. Osteoporos Int 29:69–77

    CAS  PubMed  Google Scholar 

  22. 22.

    Burt LA, Billington EO, Rose MS, Raymond DA, Hanley DA, Boyd SK (2019) Effect of high-dose vitamin D supplementation on volumetric bone density and bone strength: a randomized clinical trial. JAMA 322:736–745

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Burt LA, Schipilow JD, Boyd SK (2016) Competitive trampolining influences trabecular bone structure, bone size, and bone strength. J Sport Health Sci 5:469–475

    PubMed  Google Scholar 

  24. 24.

    Gabel L, Macdonald HM, Nettlefold L, McKay HA (2017) Physical activity, sedentary time, and bone strength from childhood to early adulthood: a mixed longitudinal HR-pQCT study. J Bone Miner Res 32:1525–1536

    CAS  PubMed  Google Scholar 

  25. 25.

    Hughes JM, Gaffney-Stomberg E, Guerriere KI, Taylor KM, Popp KL, Xu C, Unnikrishnan G, Staab JS, Matheny RW Jr, McClung JP, Reifman J, Bouxsein ML (2018) Changes in tibial bone microarchitecture in female recruits in response to 8weeks of U.S. Army Basic Combat Training. Bone 113:9–16

    PubMed  Google Scholar 

  26. 26.

    Kazakia GJ, Tjong W, Nirody JA, Burghardt AJ, Carballido-Gamio J, Patsch JM, Link T, Feeley BT, Ma CB (2014) The influence of disuse on bone microstructure and mechanics assessed by HR-pQCT. Bone 63:132–140

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Mikolajewicz N, Bishop N, Burghardt AJ et al (2019) HR-pQCT measures of bone microarchitecture predict fracture: systematic review and meta-analysis. J Bone Miner Res

  28. 28.

    Stauber M, Müller R (2008) Micro-computed tomography: a method for the non-destructive evaluation of the three-dimensional structure of biological specimens. Methods Mol Biol 455:273–292

    PubMed  Google Scholar 

  29. 29.

    Agarwal S, Rosete F, Zhang C, McMahon DJ, Guo XE, Shane E, Nishiyama KK (2016) In vivo assessment of bone structure and estimated bone strength by first- and second-generation HR-pQCT. Osteoporos Int 27:2955–2966

    CAS  PubMed  Google Scholar 

  30. 30.

    Bandirali M, Lanza E, Messina C, Sconfienza LM, Brambilla R, Maurizio R, Marchelli D, Piodi LP, di Leo G, Ulivieri FM, Sardanelli F (2013) Dose absorption in lumbar and femoral dual energy X-ray absorptiometry examinations using three different scan modalities: an anthropomorphic phantom study. J Clin Densitom 16:279–282

    PubMed  Google Scholar 

  31. 31.

    Wylie JD, Jenkins PA, Beckmann JT, Peters CL, Aoki SK, Maak TG (2018) Computed tomography scans in patients with young adult hip pain carry a lifetime risk of malignancy. Arthroscopy 34(155–163):e153

    Google Scholar 

  32. 32.

    Manske SL, Zhu Y, Sandino C, Boyd SK (2015) Human trabecular bone microarchitecture can be assessed independently of density with second generation HR-pQCT. Bone 79:213–221

    CAS  PubMed  Google Scholar 

  33. 33.

    Manske SL, Davison EM, Burt LA, Raymond DA, Boyd SK (2017) The estimation of second-generation HR-pQCT from first-generation HR-pQCT using in vivo cross-calibration. J Bone Miner Res 32:1514–1524

    PubMed  Google Scholar 

  34. 34.

    Wang Q, Wang XF, Iuliano-Burns S, Ghasem-Zadeh A, Zebaze R, Seeman E (2010) Rapid growth produces transient cortical weakness: a risk factor for metaphyseal fractures during puberty. J Bone Miner Res 25:1521–1526

    PubMed  Google Scholar 

  35. 35.

    Burrows M, Liu D, Moore S, McKay H (2010) Bone microstructure at the distal tibia provides a strength advantage to males in late puberty: an HR-pQCT study. J Bone Miner Res 25:1423–1432

    PubMed  Google Scholar 

  36. 36.

    Bonaretti S, Majumdar S, Lang TF, Khosla S, Burghardt AJ (2017) The comparability of HR-pQCT bone measurements is improved by scanning anatomically standardized regions. Osteoporos Int 28:2115–2128

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Shanbhogue VV, Hansen S, Halekoh U, Brixen K (2015) Use of relative vs fixed offset distance to define region of interest at the distal radius and tibia in high-resolution peripheral quantitative computed tomography. J Clin Densitom 18:217–225

    PubMed  Google Scholar 

  38. 38.

    Boyd SK (2008) Site-specific variation of bone micro-architecture in the distal radius and tibia. J Clin Densitom 11:424–430

    PubMed  Google Scholar 

  39. 39.

    Hauspie RC, Vercauteren M, Susanne C (1997) Secular changes in growth and maturation: an update. Acta Paediatr Suppl 423:20–27

    CAS  PubMed  Google Scholar 

  40. 40.

    Ghasem-Zadeh A, Burghardt A, Wang XF, Iuliano S, Bonaretti S, Bui M, Zebaze R, Seeman E (2017) Quantifying sex, race, and age specific differences in bone microstructure requires measurement of anatomically equivalent regions. Bone 101:206–213

    PubMed  Google Scholar 

  41. 41.

    Sode M, Burghardt AJ, Pialat JB, Link TM, Majumdar S (2011) Quantitative characterization of subject motion in HR-pQCT images of the distal radius and tibia. Bone 48:1291–1297

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Bonaretti S, Vilayphiou N, Chan CM, Yu A, Nishiyama K, Liu D, Boutroy S, Ghasem-Zadeh A, Boyd SK, Chapurlat R, McKay H, Shane E, Bouxsein ML, Black DM, Majumdar S, Orwoll ES, Lang TF, Khosla S, Burghardt AJ (2017) Operator variability in scan positioning is a major component of HR-pQCT precision error and is reduced by standardized training. Osteoporos Int 28:245–257

    CAS  PubMed  Google Scholar 

  43. 43.

    Zebaze R, Ghasem-Zadeh A, Mbala A, Seeman E (2013) A new method of segmentation of compact-appearing, transitional and trabecular compartments and quantification of cortical porosity from high resolution peripheral quantitative computed tomographic images. Bone 54:8–20

    CAS  PubMed  Google Scholar 

  44. 44.

    Schafer AL, Burghardt AJ, Sellmeyer DE, Palermo L, Shoback DM, Majumdar S, Black DM (2013) Postmenopausal women treated with combination parathyroid hormone (1-84) and ibandronate demonstrate different microstructural changes at the radius vs. tibia: the PTH and Ibandronate Combination Study (PICS). Osteoporos Int 24:2591–2601

    CAS  PubMed  Google Scholar 

  45. 45.

    Cheung AM, Majumdar S, Brixen K, Chapurlat R, Fuerst T, Engelke K, Dardzinski B, Cabal A, Verbruggen N, Ather S, Rosenberg E, de Papp AE (2014) Effects of odanacatib on the radius and tibia of postmenopausal women: improvements in bone geometry, microarchitecture, and estimated bone strength. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 29:1786–1794

    CAS  Google Scholar 

  46. 46.

    Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM (2013) Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 28:313–324

    Google Scholar 

  47. 47.

    Wong AK (2016) A comparison of peripheral imaging technologies for bone and muscle quantification: a technical review of image acquisition. J Musculoskelet Neuronal Interact 16:265–282

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Stagi S, Cavalli L, Cavalli T, de Martino M, Brandi ML (2016) Peripheral quantitative computed tomography (pQCT) for the assessment of bone strength in most of bone affecting conditions in developmental age: a review. Ital J Pediatr 42:88

    PubMed  PubMed Central  Google Scholar 

  49. 49.

    Engelke K, Stampa B, Timm W, Dardzinski B, de Papp AE, Genant HK, Fuerst T (2012) Short-term in vivo precision of BMD and parameters of trabecular architecture at the distal forearm and tibia. Osteoporos Int 23:2151–2158

    CAS  PubMed  Google Scholar 

  50. 50.

    Pauchard Y, Liphardt AM, Macdonald HM, Hanley DA, Boyd SK (2012) Quality control for bone quality parameters affected by subject motion in high-resolution peripheral quantitative computed tomography. Bone 50:1304–1310

    PubMed  Google Scholar 

  51. 51.

    Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S (2012) Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone 50:111–118

    CAS  PubMed  Google Scholar 

  52. 52.

    Laib A, Hauselmann HJ, Ruegsegger P (1998) In vivo high resolution 3D-QCT of the human forearm. Technol Health Care 6:329–337

    CAS  PubMed  Google Scholar 

  53. 53.

    Davis KA, Burghardt AJ, Link TM, Majumdar S (2007) The effects of geometric and threshold definitions on cortical bone metrics assessed by in vivo high-resolution peripheral quantitative computed tomography. Calcif Tissue Int 81:364–371

    CAS  PubMed  Google Scholar 

  54. 54.

    Nishiyama KK, Macdonald HM, Buie HR, Hanley DA, Boyd SK (2010) Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 25:882–890

    Google Scholar 

  55. 55.

    Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK (2007) Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone 41:505–515

    PubMed  Google Scholar 

  56. 56.

    Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK (2010) Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone 47:519–528

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Whittier DE, Mudryk AN, Vandergaag ID, Burt LA, Boyd SK (2019) Optimizing HR-pQCT workflow: a comparison of bias and precision error for quantitative bone analysis. Osteoporos Int

  58. 58.

    Kawalilak CE, Johnston JD, Cooper DM, Olszynski WP, Kontulainen SA (2016) Role of endocortical contouring methods on precision of HR-pQCT-derived cortical micro-architecture in postmenopausal women and young adults. Osteoporos Int 27:789–796

    CAS  PubMed  Google Scholar 

  59. 59.

    de Waard EAC, Sarodnik C, Pennings A, de Jong JJA, Savelberg HHCM, van Geel TA, van der Kallen CJ, Stehouwer CDA, Schram MT, Schaper N, Dagnelie PC, Geusens PPMM, Koster A, van Rietbergen B, van den Bergh JPW (2018) Reliability of HR-pQCT derived cortical bone structural parameters when using uncorrected instead of corrected automatically generated endocortical contours in a cross-sectional study: the Maastricht Study. Calcif Tissue Int 103:252–265

    PubMed  PubMed Central  Google Scholar 

  60. 60.

    Hildebrand T, Rüegsegger P (1997) Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Engin 1:15–23

    PubMed  Google Scholar 

  61. 61.

    Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14:1167–1174

    CAS  PubMed  Google Scholar 

  62. 62.

    Odgaard A, Gundersen HJ (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14:173–182

    CAS  PubMed  Google Scholar 

  63. 63.

    Whitehouse WJ (1974) The quantitative morphology of anisotropic trabecular bone. J Microsc 101:153–168

    CAS  PubMed  Google Scholar 

  64. 64.

    Liu XS, Sajda P, Saha PK, Wehrli FW, Bevill G, Keaveny TM, Guo XE (2008) Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J Bone Miner Res 23:223–235

    PubMed  Google Scholar 

  65. 65.

    Jorgenson BL, Buie HR, McErlain DD, Sandino C, Boyd SK (2015) A comparison of methods for in vivo assessment of cortical porosity in the human appendicular skeleton. Bone 73:167–175

    PubMed  Google Scholar 

  66. 66.

    van Rietbergen B, Ito K (2015) A survey of micro-finite element analysis for clinical assessment of bone strength: the first decade. J Biomech 48:832–841

    PubMed  Google Scholar 

  67. 67.

    MacNeil JA, Boyd SK (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213

    PubMed  Google Scholar 

  68. 68.

    Arias-Moreno AJ, Hosseini HS, Bevers M, Ito K, Zysset P, van Rietbergen B (2019) Validation of distal radius failure load predictions by homogenized- and micro-finite element analyses based on second-generation high-resolution peripheral quantitative CT images. Osteoporos Int 30:1433–1443

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P (2002) Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone 30:842–848

    CAS  PubMed  Google Scholar 

  70. 70.

    Christen D, Zwahlen A, Müller R (2014) Reproducibility for linear and nonlinear micro-finite element simulations with density derived material properties of the human radius. J Mech Behav Biomed Mater 29:500–507

    PubMed  Google Scholar 

  71. 71.

    de Jong JJ, Willems PC, Arts JJ, Bours SG, Brink PR, van Geel TA, Poeze M, Geusens PP, van Rietbergen B, van den Bergh JP (2014) Assessment of the healing process in distal radius fractures by high resolution peripheral quantitative computed tomography. Bone 64:65–74

    PubMed  Google Scholar 

  72. 72.

    Engelke K, van Rietbergen B, Zysset P (2016) FEA to measure bone strength: a review. Clinic Rev Bone Miner Metab 14:26–37

    Google Scholar 

  73. 73.

    Müller R, Rüegsegger P (1995) Three-dimensional finite element modelling of non-invasively assessed trabecular bone structures. Med Eng Phys 17:126–133

    PubMed  Google Scholar 

  74. 74.

    Whittier DE, Manske SL, Kiel DP, Bouxsein M, Boyd SK (2018) Harmonizing finite element modelling for non-invasive strength estimation by high-resolution peripheral quantitative computed tomography. J Biomech 80:63–71

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Christen D, Melton LJ 3rd, Zwahlen A, Amin S, Khosla S, Muller R (2013) Improved fracture risk assessment based on nonlinear micro-finite element simulations from HRpQCT images at the distal radius. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 28:2601–2608

    Google Scholar 

  76. 76.

    Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P (2004) Image-based micro-finite-element modeling for improved distal radius strength diagnosis: moving from bench to bedside. J Clin Densitom 7:153–160

    CAS  PubMed  Google Scholar 

  77. 77.

    Mueller TL, Christen D, Sandercott S, Boyd SK, van Rietbergen B, Eckstein F, Lochmuller EM, Muller R, van Lenthe GH (2011) Computational finite element bone mechanics accurately predicts mechanical competence in the human radius of an elderly population. Bone 48:1232–1238

    PubMed  Google Scholar 

  78. 78.

    Varga P, Pahr DH, Baumbach S, Zysset PK (2010) HR-pQCT based FE analysis of the most distal radius section provides an improved prediction of Colles’ fracture load in vitro. Bone 47:982–988

    PubMed  Google Scholar 

  79. 79.

    Kroker A, Plett R, Nishiyama KK, McErlain DD, Sandino C, Boyd SK (2017) Distal skeletal tibia assessed by HR-pQCT is highly correlated with femoral and lumbar vertebra failure loads. J Biomech 59:43–49

    PubMed  Google Scholar 

  80. 80.

    van Rietbergen B, Weinans H, Huiskes R, Odgaard A (1995) A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. J Biomech 28:69–81

    PubMed  Google Scholar 

  81. 81.

    Chen H, Zhou X, Fujita H, Onozuka M, Kubo KY (2013) Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol 2013:213234

    PubMed  PubMed Central  Google Scholar 

  82. 82.

    Seeman E, Delmas PD, Hanley DA, Sellmeyer D, Cheung AM, Shane E, Kearns A, Thomas T, Boyd SK, Boutroy S, Bogado C, Majumdar S, Fan M, Libanati C, Zanchetta J (2010) Microarchitectural deterioration of cortical and trabecular bone: differing effects of denosumab and alendronate. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 25:1886–1894

    Google Scholar 

  83. 83.

    Paggiosi MA, Eastell R, Walsh JS (2014) Precision of high-resolution peripheral quantitative computed tomography measurement variables: influence of gender, examination site, and age. Calcif Tissue Int 94:191–201

    CAS  PubMed  Google Scholar 

  84. 84.

    Ellouz R, Chapurlat R, van Rietbergen B, Christen P, Pialat JB, Boutroy S (2014) Challenges in longitudinal measurements with HR-pQCT: evaluation of a 3D registration method to improve bone microarchitecture and strength measurement reproducibility. Bone 63:147–157

    PubMed  Google Scholar 

  85. 85.

    Nishiyama KK, Pauchard Y, Nikkel LE, Iyer S, Zhang C, McMahon DJ, Cohen D, Boyd SK, Shane E, Nickolas TL (2015) Longitudinal HR-pQCT and image registration detects endocortical bone loss in kidney transplantation patients. J Bone Miner Res 30:554–561

    PubMed  Google Scholar 

  86. 86.

    Adams JE, Engelke K, Zemel BS, Ward KA, International Society of Clinical D (2014) Quantitative computer tomography in children and adolescents: the 2013 ISCD Pediatric Official Positions. J Clin Densitom 17:258–274

    PubMed  Google Scholar 

  87. 87.

    de Jong JJA, Christen P, Plett RM, Chapurlat R, Geusens PP, van den Bergh JPW, Müller R, van Rietbergen B (2017) Feasibility of rigid 3D image registration of high-resolution peripheral quantitative computed tomography images of healing distal radius fractures. PLoS One 12:e0179413

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    Chiba K, Okazaki N, Kurogi A, Isobe Y, Yonekura A, Tomita M, Osaki M (2018) Precision of second-generation high-resolution peripheral quantitative computed tomography: intra- and intertester reproducibilities and factors involved in the reproducibility of cortical porosity. J Clin Densitom 21:295–302

    PubMed  Google Scholar 

  89. 89.

    Shepherd JA, Lu Y (2007) A generalized least significant change for individuals measured on different DXA systems. J Clin Densitom 10:249–258

    PubMed  Google Scholar 

  90. 90.

    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300

    Google Scholar 

  91. 91.

    Boutroy S, Khosla S, Sornay-Rendu E, Zanchetta MB, McMahon DJ, Zhang CA, Chapurlat RD, Zanchetta J, Stein EM, Bogado C, Majumdar S, Burghardt AJ, Shane E (2016) Microarchitecture and peripheral BMD are impaired in postmenopausal white women with fracture independently of total hip T-score: an international multicenter study. J Bone Miner Res 31:1158–1166

    CAS  PubMed  PubMed Central  Google Scholar 

  92. 92.

    Yekutieli D (2008) Hierarchical flse discovery rate-controlling methodology. J Am Stat Assoc 103:309–316

    CAS  Google Scholar 

  93. 93.

    Gensburger D, Boutroy S, Chapurlat R, Nove-Josserand R, Roche S, Rabilloud M, Durieu I (2016) Reduced bone volumetric density and weak correlation between infection and bone markers in cystic fibrosis adult patients. Osteoporos Int 27:2803–2813

    CAS  PubMed  Google Scholar 

  94. 94.

    Burghardt AJ, Pialat JB, Kazakia GJ, Boutroy S, Engelke K, Patsch JM, Valentinitsch A, Liu D, Szabo E, Bogado CE, Zanchetta MB, McKay HA, Shane E, Boyd SK, Bouxsein ML, Chapurlat R, Khosla S, Majumdar S (2013) Multicenter precision of cortical and trabecular bone quality measures assessed by high-resolution peripheral quantitative computed tomography. J Bone Miner Res 28:524–536

    PubMed  PubMed Central  Google Scholar 

  95. 95.

    Cauley JA, Burghardt AJ, Harrison SL, Cawthon PM, Schwartz AV, Connor EB, Ensrud KE, Langsetmo L, Majumdar S, Orwoll E, for the Osteoporotic Fractures in Men (MrOS) Research Group (2018) Accelerated bone loss in older men: effects on bone microarchitecture and strength. J Bone Miner Res 33:1859–1869

    CAS  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Caksa S, Yuan A, Rudolph SE, Yu EW, Popp KL, Bouxsein ML (2019) Influence of soft tissue on bone density and microarchitecture measurements by high-resolution peripheral quantitative computed tomography. Bone 124:47–52

    PubMed  Google Scholar 

  97. 97.

    de Jong JJ, Arts JJ, Meyer U, Willems PC, Geusens PP, van den Bergh JP, van Rietbergen B (2016) Effect of a cast on short-term reproducibility and bone parameters obtained from HR-pQCT measurements at the distal end of the radius. J Bone Joint Surg Am 98:356–362

    PubMed  Google Scholar 

  98. 98.

    Whittier DE, Manske SL, Boyd SK, Schneider PS (2018) The correction of systematic error due to plaster and fiberglass casts on HR-pQCT bone parameters measured in vivo at the distal radius. J Clin Densitom

  99. 99.

    MacNeil JA, Boyd SK (2007) Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 29:1096–1105

    PubMed  Google Scholar 

  100. 100.

    de Charry C, Boutroy S, Ellouz R, Duboeuf F, Chapurlat R, Follet H, Pialat JB (2016) Clinical cone beam computed tomography compared to high-resolution peripheral computed tomography in the assessment of distal radius bone. Osteoporos Int 27:3073–3082

    PubMed  Google Scholar 

  101. 101.

    Klintstrom E, Smedby O, Moreno R, Brismar TB (2014) Trabecular bone structure parameters from 3D image processing of clinical multi-slice and cone-beam computed tomography data. Skelet Radiol 43:197–204

    Google Scholar 

  102. 102.

    Mys K, Varga P, Gueorguiev B, Hemmatian H, Stockmans F, van Lenthe GH (2019) Correlation between cone-beam computed tomography and high-resolution peripheral computed tomography for assessment of wrist bone microstructure. J Bone Miner Res 34:867–874

    PubMed  Google Scholar 

  103. 103.

    Brehler M, Cao Q, Moseley KF, Osgood G, Morris C, Demehri S, Yorkston J, Siewerdsen JH, Zbijewski W (2018) Robust quantitative assessment of trabecular microarchitecture in extremity cone-beam CT using optimized segmentation algorithms. Proc SPIE Int Soc Opt Eng 10578:

  104. 104.

    Kawalilak CE, Bunyamin AT, Bjorkman KM, Johnston JD, Kontulainen SA (2017) Precision of bone density and micro-architectural properties at the distal radius and tibia in children: an HR-pQCT study. Osteoporos Int 28:3189–3197

    CAS  PubMed  Google Scholar 

  105. 105.

    Kroker A, Besler BA, Bhatla JL, Shtil M, Salat P, Mohtadi N, Walker RE, Manske SL, Boyd SK (2019) Longitudinal effects of acute anterior cruciate ligament tears on peri-articular bone in human knees within the first year of injury. J Orthop Res 37:2325–2336

    PubMed  Google Scholar 

  106. 106.

    Burghardt AJ, Lee CH, Kuo D, Majumdar S, Imboden JB, Link TM, Li X (2013) Quantitative in vivo HR-pQCT imaging of 3D wrist and metacarpophalangeal joint space width in rheumatoid arthritis. Ann Biomed Eng 41:2553–2564

    PubMed  Google Scholar 

  107. 107.

    Nagaraj S, Finzel S, Stok KS, Barnabe C, Collaboration S (2016) High-resolution peripheral quantitative computed tomography imaging in the assessment of periarticular bone of metacarpophalangeal and wrist joints. J Rheumatol 43:1921–1934

    PubMed  Google Scholar 

  108. 108.

    Kroker A, Zhu Y, Manske SL, Barber R, Mohtadi N, Boyd SK (2017) Quantitative in vivo assessment of bone microarchitecture in the human knee using HR-pQCT. Bone 97:43–48

    PubMed  Google Scholar 

  109. 109.

    Manske SL, Brunet SC, Finzel S, Stok KS, Conaghan PG, Boyd SK, Barnabe C (2019) The SPECTRA collaboration OMERACT working group: construct validity of joint space outcomes with high-resolution peripheral quantitative computed tomography. J Rheumatol 46:1369–1373

    PubMed  Google Scholar 

  110. 110.

    Stok KS, Finzel S, Burghardt AJ, Conaghan PG, Barnabe C, Collaboration S (2017) The SPECTRA collaboration OMERACT special interest group: current research and future directions. J Rheumatol 44:1911–1915

    PubMed  Google Scholar 

  111. 111.

    Vilayphiou N, Boutroy S, Sornay-Rendu E, Van Rietbergen B, Munoz F, Delmas PD, Chapurlat R (2010) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in postmenopausal women. Bone 46:1030–1037

    PubMed  Google Scholar 

  112. 112.

    Hosseini HS, Dunki A, Fabech J, Stauber M, Vilayphiou N, Pahr D, Pretterklieber M, Wandel J, Rietbergen BV, Zysset PK (2017) Fast estimation of Colles’ fracture load of the distal section of the radius by homogenized finite element analysis based on HR-pQCT. Bone 97:65–75

    PubMed  Google Scholar 

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Correspondence to M.L. Bouxsein.

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Dr. Boyd is a co-founder and co-owner of Numerics88 Solutions Inc., creator of finite element package FAIM. Dr. Ghasem-Zadeh is one of the inventors of the StrAx algorithm and consults for Strax Corp. Dr. Burghardt is a consultant and served on an Advisory Board to Mereo BioPharma.

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Whittier, D., Boyd, S., Burghardt, A. et al. Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int 31, 1607–1627 (2020). https://doi.org/10.1007/s00198-020-05438-5

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Keywords

  • Bone microarchitecture
  • Guidelines
  • High-resolution peripheral quantitative computed tomography
  • Imaging protocol