Advertisement

Current Osteoporosis Reports

, Volume 16, Issue 6, pp 665–673 | Cite as

PET-MRI for the Study of Metabolic Bone Disease

  • James S. Yoder
  • Feliks Kogan
  • Garry E. Gold
Imaging (T Lang and F Wehrli, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Imaging

Abstract

Purpose of Review

This review article attempts to summarize the current state and applications of the hybrid imaging modality of PET-MRI to metabolic bone diseases. The advances of PET and MRI are also discussed for metabolic bone diseases as potentially applied via PET-MRI.

Recent Findings

Etiologies and mechanisms of metabolic bone disease can be complex where molecular changes precede structural changes. Although PET-MRI has yet to be applied directly to metabolic bone disease, possible applications exist since PET, specifically 18F-NaF PET, can quantitatively track changes in bone metabolism and is useful for assessing treatment, while MRI can give detailed information on bone water concentration, porosity, and architecture through novel techniques such as UTE and ZTE MRI.

Summary

Earlier detection and further understanding of metabolic bone disease via PET and MRI could lead to better treatment and prevention. More research using this modality is needed to further understand how it can be implemented in this realm.

Keywords

Positron emission tomography-magnetic resonance imaging (PET-MRI) Musculoskeletal diseases Metabolic bone disease Imaging 

Notes

Compliance with Ethical Standards

Conflict of Interest

James Yoder, Feliks Kogan and Garry Gold report grants from GE Healthcare and the NIH during the conduct of this study.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Disclosure Statement

The authors receive research support from GE Healthcare.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Chen K, Blebea J, Laredo JD, Chen W, Alavi A, Torigian DA. Evaluation of musculoskeletal disorders with PET, PET/CT, and PET/MRI. PET Clin. 2008;3(3):451–65.CrossRefGoogle Scholar
  2. 2.
    Kogan F, Fan AP, Gold GE. Potential of PET-MRI for imaging of non-oncologic musculoskeletal disease. Quant Imaging Med Surg. 2016;6(6):756–71.CrossRefGoogle Scholar
  3. 3.
    Wainwright SA, Marshall LM, Ensrud KE, Cauley JA, Black DM, Hillier TA, et al. Hip fracture in women without osteoporosis. J Clin Endocrinol Metab. 2005;90:2787–93.CrossRefGoogle Scholar
  4. 4.
    Griffeth LK. Use of PET/CT scanning in cancer patients: technical and practical considerations. Proc (Baylor Univ Med Cent). 2005;18:321–30.CrossRefGoogle Scholar
  5. 5.
    Hirsch FW, Sattler B, Sorge I, Kurch L, Viehweger A, Ritter L, et al. PET/MR in children. Initial clinical experience in paediatric oncology using an integrated PET/MR scanner. Pediatr Radiol. 2013;43:860–75.CrossRefGoogle Scholar
  6. 6.
    Huang B, Law MWM, Khong PL. Whole-body PET/CT scanning: estimation of radiation dose and cancer risk. Radiology. 2009;251:166–74.CrossRefGoogle Scholar
  7. 7.
    Judenhofer MS, Wehrl HF, Newport DF, Catana C, Siegel SB, Becker M, et al. Simultaneous PET-MRI: a new approach for functional and morphological imaging. Nat Med. 2008;14:459–65.CrossRefGoogle Scholar
  8. 8.
    Chaudhry AA, Gul M, Gould E, Teng M, Baker K, Matthews R. Utility of positron emission tomography-magnetic resonance imaging in musculoskeletal imaging. World J Radiol. 2016;8:268–74.CrossRefGoogle Scholar
  9. 9.
    Jadvar H, Desai B, Conti PS. Sodium 18F-fluoride PET/CT of bone, joint, and other disorders. Semin Nucl Med. 2015;45(1):58–65.CrossRefGoogle Scholar
  10. 10.
    Czernin J, Satyamurthy N, Schiepers C. Molecular mechanisms of bone 18F-NaF deposition. J Nucl Med. 2010;51(12):1826–9.CrossRefGoogle Scholar
  11. 11.
    Etchebehere EC, Hobbs BP, Milton DR, Malawi O, Patel S, Benjamin RS, et al. Assessing the role of (1)(8)F-FDG PET and (1)(8)F-FDG PET/CT in the diagnosis of soft tissue musculoskeletal malignancies: a systematic review and meta-analysis. Eur J Nucl Med Mol Imaging. 2016;43:860–70.CrossRefGoogle Scholar
  12. 12.
    Schelbert HR, Hoh CK, Royal HD, et al. Procedure guideline for tumor imaging using fluorine-18-FDG. Society of Nuclear Medicine. J Nucl Med. 1998;39:1302–5.PubMedGoogle Scholar
  13. 13.
    Crymes WB Jr, Demos H, Gordon L. Detection of musculoskeletal infection with 18F-FDG PET: review of the current literature. J Nucl Med Technol. 2004;32:12–5.PubMedGoogle Scholar
  14. 14.
    Raynor W, Houshmand S, Alavi A, et al. Evolving role of molecular imaging with (18)F-sodium fluoride PET as a biomarker for calcium metabolism. Curr Osteoporos Rep. 2016;14:115–25.CrossRefGoogle Scholar
  15. 15.
    Blake GM, Siddique M, Frost ML, Moore AEB, Fogelman I. Imaging of site specific bone turnover in osteoporosis using positron emission tomography. Curr Osteoporos Rep. 2014;12(4):475–85.CrossRefGoogle Scholar
  16. 16.
    Schiepers C, Nuyts J, Bormans G, et al. Fluoride kinetics of the axial skeleton measured in vivo with fluorine-18-fluoride PET. J Nucl Med. 1997;38:1970–6.PubMedGoogle Scholar
  17. 17.
    Kobayashi N, Inaba Y, Tateishi U, Yukizawa Y, Ike H, Inoue T, et al. New application of 18F-fluoride PET for the detection of bone remodeling in early-stage osteoarthritis of the hip. Clin Nucl Med. 2013;38:e379–83.CrossRefGoogle Scholar
  18. 18.
    Blau M, Ganatra R, Bender MA. 18 F-fluoride for bone imaging. Semin Nucl Med. 1972;2:31–7.CrossRefGoogle Scholar
  19. 19.
    Uchida K, Nakajima H, Miyazaki T, et al. Effects of alendronate on bone metabolism in glucocorticoid-induced osteoporosis measured by 18F-fluoride PET: a prospective study. J Nucl Med Off Publ Soc Nucl Med. 2009;50(11):1808–14.Google Scholar
  20. 20.
    Bentourkia M, Zaidi H. Tracer kinetic modeling in PET. PET Clin. 2007;2(2):267–77.CrossRefGoogle Scholar
  21. 21.
    Hawkins RA, Choi Y, Huang SC, et al. Evaluation of the skeletal kinetics of fluorine-18-fluoride ion with PET. J Nucl Med. 1992;33:633–42.PubMedGoogle Scholar
  22. 22.
    Frost ML, Cook GJR, Blake GM, Marsden PK, Benatar NA, Fogelman I. A prospective study of risedronate on regional bone metabolism and blood flow at the lumbar spine measured by 18F-fluoride positron emission tomography. J Bone Miner Res. 2003;18:2215–22.CrossRefGoogle Scholar
  23. 23.
    Frost ML, Siddique M, Blake GM, Moore AEB, Schleyer PJ, Dunn JT, et al. Differential effects of teriparatide on regional bone formation using 18F-fluoride positron emission tomography. J Bone Miner Res. 2011;26:1002–11.CrossRefGoogle Scholar
  24. 24.
    Cook GJ, Lodge MA, Marsden PK, et al. Non-invasive assessment of skeletal kinetics using fluorine-18 fluoride positron emission tomography: evaluation of image and population-derived arterial input functions. Eur J Nucl Med. 1999;26:1424–9.CrossRefGoogle Scholar
  25. 25.
    Installe J, Nzeusseu A, Bol A, et al. 18F-fluoride PET for monitoring therapeutic response in Paget’s disease of bone. J Nucl Med. 2005;46:1650–8.PubMedGoogle Scholar
  26. 26.
    • Blake GM, Siddique M, Frost ML, Moore AE, Fogelman I. Quantitative PET imaging using 18F sodium fluoride in the assessment of metabolic bone diseases and the monitoring of their response to therapy. PET Clin. 2012;7:275–91 The article discusses how 18F-NaF PET can be used to quantify bone metabolism and monitor responses to treatments through bone plasma clearance and SUV measurements. CrossRefGoogle Scholar
  27. 27.
    Blake GM, Frost ML, Fogelman I. Quantitative radionuclide studies of bone. J Nucl Med. 2009;50:1747–50.CrossRefGoogle Scholar
  28. 28.
    • Kogan F, Fan AP, McWalter EJ, et al. PET/MRI of metabolic activity in osteoarthritis: a feasibility study. J Magn Reson Imaging. 2017;45(6):1736–45 This study demonstrates how hybrid PET-MRI can be used to detect metabolic bone abnormalities in osteoarthritis and could be applied specifically to metabolic bone diseases. CrossRefGoogle Scholar
  29. 29.
    Menendez MI, Hettlich B, Wei L, Knopp MV. Feasibility of Na18F PET/CT and MRI for noninvasive in vivo quantification of knee pathophysiological bone metabolism in a canine model of post-traumatic osteoarthritis. Mol Imaging. 2017;16:1536012117714575.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Kogan F, Fan AP, Black M, Hargreaves B, Gold G. Imaging of bone metabolism and its spatial relationship with cartilage matrix changes in ACL-injured patients. Orthopaedic Research Society 2018 Annual meeting. New Orleans, LA 2018.Google Scholar
  31. 31.
    Crönlein M, Rauscher I, Beer AJ, Schwaiger M, Schäffeler C, Beirer M, et al. Visualization of stress fractures of the foot using PET-MRI: a feasibility study. Eur J Med Res. 2015;20:99.CrossRefGoogle Scholar
  32. 32.
    Fogelman I, Bessent R. Age-related alterations in skeletal metabolism-24-hr whole-body retention of diphosphonate in 250 normal subjects: concise communication. J Nucl Med. 1982;23:296–300.PubMedGoogle Scholar
  33. 33.
    Thomsen K, Johansen J, Nilas L, et al. Whole body retention of 99mTc-diphosphonate. Relation to biochemical indices of bone turnover and to total body calcium. Eur J Nucl Med. 1987;13:32–5.CrossRefGoogle Scholar
  34. 34.
    van Staa TP, Leufkens HG, Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int. 2002;13:777–87.CrossRefGoogle Scholar
  35. 35.
    Canalis E, Delany AM. Mechanisms of glucocorticoid action in bone. Ann N Y Acad Sci. 2002;966:73–81.CrossRefGoogle Scholar
  36. 36.
    Rubin MR, Bilezikian JP. Clinical review 151: the role of parathyroid hormone in the pathogenesis of glucocorticoid-induced osteoporosis: a re-examination of the evidence. J Clin Endocrinol Metab. 2002;87(9):4033–41.CrossRefGoogle Scholar
  37. 37.
    Blake GM, Park-Holohan SJ, Fogelman I. Quantitative studies of bone in postmenopausal women using (18)F-fluoride and (99m)Tc-methylene diphosphonate. J Nucl Med. 2002;43:338–45.PubMedGoogle Scholar
  38. 38.
    Kato K, Aoki J, Endo K. Utility of FDG-PET in differential diagnosis of benign and malignant fractures in acute to subacute phase. Ann Nucl Med. 2003;17:41–6.CrossRefGoogle Scholar
  39. 39.
    Schmitz A, Risse JH, Textor J, Zander D, Biersack HJ, Schmitt O, et al. FDG-PET findings of vertebral compression fractures in osteoporosis: preliminary results. Osteoporos Int. 2002;13:755–61.CrossRefGoogle Scholar
  40. 40.
    Patsch JM, Li X, Baum T, Yap SP, Karampinos DC, Schwartz AV, et al. Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J Bone Miner Res. 2013;28:1721–8.CrossRefGoogle Scholar
  41. 41.
    Huovinen V, Saunavaara V, Parkkola R, et al. Vertebral bone marrow glucose uptake is inversely associated with bone marrow fat in diabetic and healthy pigs: [(18)F]FDG-PET and MRI study. Bone. 2014;61:33–8.CrossRefGoogle Scholar
  42. 42.
    Agrawal K, Agarwal Y, Chopra RK, et al. Evaluation of MR spectroscopy and diffusion-weighted MRI in postmenopausal bone strength. Cureus. 2015;e327:7.Google Scholar
  43. 43.
    Schwartz AV, Sigurdsson S, Hue TF, Lang TF, Harris TB, Rosen CJ, et al. Vertebral bone marrow fat associated with lower trabecular BMD and prevalent vertebral fracture in older adults. J Clin Endocrinol Metab. 2013;98:2294–300.CrossRefGoogle Scholar
  44. 44.
    Messa C, Goodman WG, Hoh CK, et al. Bone metabolic activity measured with positron emission tomography and [18F]fluoride ion in renal osteodystrophy: correlation with bone histomorphometry. J Clin Endocrinol Metab. 1993;77:949–55.PubMedGoogle Scholar
  45. 45.
    Usmani S, Marafi F, Esmail A, Ahmed N. A proof-of-concept study analyzing the clinical utility of fluorine-18-sodium fluoride PET-CT in skeletal staging of oncology patients with end-stage renal disease on dialysis. Nucl Med Commun. 2017;38(12):1067–75.CrossRefGoogle Scholar
  46. 46.
    Meunier PJ, Coindre JM, Edouard CM, Arlot ME. Bone histomorphometry in Paget’s disease. Quantitative and dynamic analysis of pagetic and nonpagetic bone tissue. Arthritis Rheum. 1980;23:1095–103.CrossRefGoogle Scholar
  47. 47.
    Cook GJ, Blake GM, Marsden PK, et al. Quantification of skeletal kinetic indices in Paget’s disease using dynamic 18F-fluoride positron emission tomography. J Bone Miner Res. 2002;17:854–9.CrossRefGoogle Scholar
  48. 48.
    Devogelaer JP. Modern therapy for Paget’s disease of bone: focus on bisphosphonates. Treat Endocrinol. 2002;1:241–57.CrossRefGoogle Scholar
  49. 49.
    Cook GJ, Lodge MA, Blake GM, et al. Differences in skeletal kinetics between vertebral and humeral bone measured by 18F-fluoride positron emission tomography in postmenopausal women. J Bone Miner Res. 2000;15:763–9.CrossRefGoogle Scholar
  50. 50.
    Bala Y, Zebaze R, Seeman E. Role of cortical bone in bone fragility. Curr Opin Rheumatol. 2015;27:406–513.CrossRefGoogle Scholar
  51. 51.
    Bala Y, Zebaze R, Seeman E, et al. Cortical porosity identifies women with osteopenia at increased risk for forearm fractures. J Bone Miner Res. 2014;29:1356–62.CrossRefGoogle Scholar
  52. 52.
    Ahmed LA, Shigdel R, Bjørnerem Å, et al. Measurement of cortical porosity of the proximal femur improves identification of women with nonvertebral fragility fractures. Osteoporos Int. 2015;26:2137–46.CrossRefGoogle Scholar
  53. 53.
    Li C, Seifert AC, Wehrli FW, et al. Cortical bone water concentration: dependence of MR imaging measures on age and pore volume fraction. Radiology. 2014;272:796–806.CrossRefGoogle Scholar
  54. 54.
    Ito M. Recent progress in bone imaging for osteoporosis research. J Bone Miner Metab. 2011;29:131–40.CrossRefGoogle Scholar
  55. 55.
    Rajapakse CS, Bashoor-Zadeh M, Li C, Sun W, Wright AC, Wehrli FW. Volumetric cortical bone porosity assessment with MR imaging: validation and clinical feasibility. Radiology. 2015;276:526–35.CrossRefGoogle Scholar
  56. 56.
    Ni Q, Nyman JS, Wang X, Santos ADL, Nicolella DP. Assessment of water distribution changes in human cortical bone by nuclear magnetic resonance. Meas Sci Technol. 2007;18:715–23.CrossRefGoogle Scholar
  57. 57.
    Techawiboonwong A, Song HK, Leonard MB, Wehrli FW. Cortical bone water: in vivo quantification with ultrashort echo-time MR imaging. Radiology. 2008;248:824–33.CrossRefGoogle Scholar
  58. 58.
    Anumula S, Wehrli SL, Magland J, Wright AC, Wehrli FW. Ultra-short echo-time MRI detects changes in bone mineralization and water content in OVX rat bone in response to alendronate treatment. Bone. 2010;46:1391–9.CrossRefGoogle Scholar
  59. 59.
    • Wiesinger F, Sacolick LI, Menini A, Zero TE, et al. MR bone imaging in the head. Magn Reson Med. 2016;75:107–14 This study demonstrates how zTE MRI can be used to distinguish bone and could be useful in MR-based attenuation correction of PET data, as it pertains to PET-MRI and metabolic bone diseases. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • James S. Yoder
    • 1
  • Feliks Kogan
    • 1
  • Garry E. Gold
    • 1
    • 2
    • 3
  1. 1.Department of RadiologyStanford UniversityStanfordUSA
  2. 2.BioengineeringStanford UniversityStanfordUSA
  3. 3.Orthopaedic SurgeryStanford UniversityStanfordUSA

Personalised recommendations