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Bone loss at the distal femur and proximal tibia in persons with spinal cord injury: imaging approaches, risk of fracture, and potential treatment options

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Abstract

Persons with spinal cord injury (SCI) undergo immediate unloading of the skeleton and, as a result, have severe bone loss below the level of lesion associated with increased risk of long-bone fractures. The pattern of bone loss in individuals with SCI differs from other forms of secondary osteoporosis because the skeleton above the level of lesion remains unaffected, while marked bone loss occurs in the regions of neurological impairment. Striking demineralization of the trabecular epiphyses of the distal femur (supracondylar) and proximal tibia occurs, with the knee region being highly vulnerable to fracture because many accidents occur while sitting in a wheelchair, making the knee region the first point of contact to any applied force. To quantify bone mineral density (BMD) at the knee, dual energy x-ray absorptiometry (DXA) and/or computed tomography (CT) bone densitometry are routinely employed in the clinical and research settings. A detailed review of imaging methods to acquire and quantify BMD at the distal femur and proximal tibia has not been performed to date but, if available, would serve as a reference for clinicians and researchers. This article will discuss the risk of fracture at the knee in persons with SCI, imaging methods to acquire and quantify BMD at the distal femur and proximal tibia, and treatment options available for prophylaxis against or reversal of osteoporosis in individuals with SCI.

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Abbreviations

SCI:

Spinal cord injury

DXA:

Dual energy x-ray absorptiometry

CT:

Computed tomography

MRI:

Magnetic resonance imaging

QCT:

Quantitative computed tomography

MDCT:

Multidetector computed tomography

pQCT:

Peripheral quantitative computerized tomography

HR-pQCT:

High-resolution peripheral quantitative computed tomography

mSv:

Millisievert

DF:

Distal femur

PT:

Proximal tibia

LE:

Lower extremity

ROI:

Region of interest

RMS-CV%:

Root mean square coefficient of variation percent

LSC:

Least significant change

BMC:

Bone mineral content

aBMD:

Areal bone mineral density

vBMD:

Volumetric bone mineral density

vBMDTb :

Trabecular volumetric bone mineral density

vBMDCt :

Cortical volumetric bone mineral density

App:

Apparent

BV/TV:

Bone volume/tissue volume

Tb.N:

Trabecular number

Tb.Sp:

Trabecular spacing

Tb.Th:

Trabecular thickness

SSIpol :

Polar stress strain index

PI:

Polar moment of inertia

ES:

Electrical stimulation

FES:

Functional electrical stimulation

ZA:

Zoledronic acid

IOF:

International Osteoporosis Foundation

AIS:

American Spinal Injury Association Impairment Scale

References

  1. Minaire P, Neunier P, Edouard C, Bernard J, Courpron P, Bourret J (1974) Quantitative histological data on disuse osteoporosis: comparison with biological data. Calcif Tissue Res 17(1):57–73

    Article  PubMed  CAS  Google Scholar 

  2. Bauman WA, Cardozo CP (2015) Osteoporosis in individuals with spinal cord injury. PM & R: the journal of injury, function, and rehabilitation 7(2):188–201 . doi:10.1016/j.pmrj.2014.08.948quiz 201

    Article  Google Scholar 

  3. Chantraine A, Nusgens B, Lapiere CM (1986) Bone remodeling during the development of osteoporosis in paraplegia. Calcif Tissue Int 38(6):323–327

    Article  PubMed  CAS  Google Scholar 

  4. Roberts D, Lee W, Cuneo RC, Wittmann J, Ward G, Flatman R, McWhinney B, Hickman PE (1998) Longitudinal study of bone turnover after acute spinal cord injury. J Clin Endocrinol Metab 83(2):415–422. doi:10.1210/jcem.83.2.4581

    Article  PubMed  CAS  Google Scholar 

  5. Shields RK, Dudley-Javoroski S, Boaldin KM, Corey TA, Fog DB, Ruen JM (2006) Peripheral quantitative computed tomography: measurement sensitivity in persons with and without spinal cord injury. Arch Phys Med Rehabil 87(10):1376–1381. doi:10.1016/j.apmr.2006.07.257

    Article  PubMed  PubMed Central  Google Scholar 

  6. Biering-Sorensen F, Bohr HH, Schaadt OP (1990) Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury. Eur J Clin Investig 20(3):330–335

    Article  CAS  Google Scholar 

  7. Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P (1995) Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia 33(11):674–677. doi:10.1038/sc.1995.141

    Article  PubMed  CAS  Google Scholar 

  8. Dauty M, Perrouin Verbe B, Maugars Y, Dubois C, Mathe JF (2000) Supralesional and sublesional bone mineral density in spinal cord-injured patients. Bone 27(2):305–309

    Article  PubMed  CAS  Google Scholar 

  9. Morse LR, Battaglino RA, Stolzmann KL, Hallett LD, Waddimba A, Gagnon D, Lazzari AA, Garshick E (2009) Osteoporotic fractures and hospitalization risk in chronic spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 20(3):385–392. doi:10.1007/s00198-008-0671-6

    Article  CAS  Google Scholar 

  10. Ingram RR, Suman RK, Freeman PA (1989) Lower limb fractures in the chronic spinal cord injured patient. Paraplegia 27(2):133–139. doi:10.1038/sc.1989.20

    Article  PubMed  CAS  Google Scholar 

  11. Ragnarsson KT, Sell GH (1981) Lower extremity fractures after spinal cord injury: a retrospective study. Arch Phys Med Rehabil 62(9):418–423

    PubMed  CAS  Google Scholar 

  12. Carbone LD, Chin AS, Burns SP, Svircev JN, Hoenig H, Heggeness M, Weaver F (2013) Morbidity following lower extremity fractures in men with spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 24(8):2261–2267. doi:10.1007/s00198-013-2295-8

    Article  CAS  Google Scholar 

  13. Akhigbe T, Chin AS, Svircev JN, Hoenig H, Burns SP, Weaver FM, Bailey L, Carbone L (2015) A retrospective review of lower extremity fracture care in patients with spinal cord injury. J Spinal cord Med 38(1):2–9. doi:10.1179/2045772313Y.0000000156

    Article  PubMed  PubMed Central  Google Scholar 

  14. Frey-Rindova P, de Bruin ED, Stussi E, Dambacher MA, Dietz V (2000) Bone mineral density in upper and lower extremities during 12 months after spinal cord injury measured by peripheral quantitative computed tomography. Spinal Cord 38(1):26–32

    Article  PubMed  CAS  Google Scholar 

  15. de Bruin ED, Vanwanseele B, Dambacher MA, Dietz V, Stussi E (2005) Long-term changes in the tibia and radius bone mineral density following spinal cord injury. Spinal Cord 43(2):96–101. doi:10.1038/sj.sc.3101685

    Article  PubMed  Google Scholar 

  16. Warden SJ, Bennell KL, Matthews B, Brown DJ, McMeeken JM, Wark JD (2002) Quantitative ultrasound assessment of acute bone loss following spinal cord injury: a longitudinal pilot study. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 13(7):586–592. doi:10.1007/s001980200077

  17. Frotzler A, Berger M, Knecht H, Eser P (2008) Bone steady-state is established at reduced bone strength after spinal cord injury: a longitudinal study using peripheral quantitative computed tomography (pQCT). Bone 43(3):549–555. doi:10.1016/j.bone.2008.05.006

    Article  PubMed  Google Scholar 

  18. Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H (2004) Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 34(5):869–880. doi:10.1016/j.bone.2004.01.001

    Article  PubMed  CAS  Google Scholar 

  19. Bauman WA, Spungen AM, Wang J, Pierson RN Jr, Schwartz E (1999) Continuous loss of bone during chronic immobilization: a monozygotic twin study. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 10(2):123–127

    Article  CAS  Google Scholar 

  20. Modlesky CM, Majumdar S, Narasimhan A, Dudley GA (2004) Trabecular bone microarchitecture is deteriorated in men with spinal cord injury. J Bone Miner Res Off J Am Soc Bone Miner Res 19(1):48–55. doi:10.1359/JBMR.0301208

    Article  Google Scholar 

  21. Recker R, Lappe J, Davies K, Heaney R (2000) Characterization of perimenopausal bone loss: a prospective study. J Bone Miner Res Off J Am Soc Bone Miner Res 15(10):1965–1973. doi:10.1359/jbmr.2000.15.10.1965

    Article  CAS  Google Scholar 

  22. Leblanc AD, Schneider VS, Evans HJ, Engelbretson DA, Krebs JM (1990) Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res Off J Am Soc Bone Miner Res 5(8):843–850. doi:10.1002/jbmr.5650050807

    Article  CAS  Google Scholar 

  23. Vico L, Collet P, Guignandon A, Lafage-Proust MH, Thomas T, Rehaillia M, Alexandre C (2000) Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet 355(9215):1607–1611

    Article  PubMed  CAS  Google Scholar 

  24. Khoo BC, Brown K, Cann C, Zhu K, Henzell S, Low V, Gustafsson S, Price RI, Prince RL (2009) Comparison of QCT-derived and DXA-derived areal bone mineral density and T scores. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 20(9):1539–1545. doi:10.1007/s00198-008-0820-y

    Article  CAS  Google Scholar 

  25. Li N, Li XM, Xu L, Sun WJ, Cheng XG, Tian W (2013) Comparison of QCT and DXA: osteoporosis detection rates in postmenopausal women. Int J Endocrinol 2013:895474. doi:10.1155/2013/895474

    Article  PubMed  PubMed Central  Google Scholar 

  26. del Puente A, Pappone N, Mandes MG, Mantova D, Scarpa R, Oriente P (1996) Determinants of bone mineral density in immobilization: a study on hemiplegic patients. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 6(1):50–54

    Article  Google Scholar 

  27. Troy KL, Morse LR (2015) Measurement of bone: diagnosis of SCI-induced osteoporosis and fracture risk prediction. Topics in spinal cord injury rehabilitation 21(4):267–274. doi:10.1310/sci2104-267

    Article  PubMed  PubMed Central  Google Scholar 

  28. Edwards WB, Schnitzer TJ, Troy KL (2014) Bone mineral and stiffness loss at the distal femur and proximal tibia in acute spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 25(3):1005–1015. doi:10.1007/s00198-013-2557-5

    Article  CAS  Google Scholar 

  29. Biering-Sorensen F, Bohr H, Schaadt O (1988) Bone mineral content of the lumbar spine and lower extremities years after spinal cord lesion. Paraplegia 26(5):293–301

    PubMed  CAS  Google Scholar 

  30. Garland DE, Adkins RH, Stewart CA (2005) Fracture threshold and risk for osteoporosis and pathologic fractures in individuals with spinal cord injury. Top Spinal Cord Inj 11(1):61–69

    Article  Google Scholar 

  31. Garland DE, Adkins RH, Stewart CA, Ashford R, Vigil D (2001) Regional osteoporosis in women who have a complete spinal cord injury. J Bone Joint Surg Am 83-A(8):1195–1200

    Article  PubMed  CAS  Google Scholar 

  32. Shields RK, Schlechte J, Dudley-Javoroski S, Zwart BD, Clark SD, Grant SA, Mattiace VM (2005) Bone mineral density after spinal cord injury: a reliable method for knee measurement. Arch Phys Med Rehabil 86(10):1969–1973. doi:10.1016/j.apmr.2005.06.001

    Article  PubMed  PubMed Central  Google Scholar 

  33. Lala D, Craven BC, Thabane L, Papaioannou A, Adachi JD, Popovic MR, Giangregorio LM (2014) Exploring the determinants of fracture risk among individuals with spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 25(1):177–185. doi:10.1007/s00198-013-2419-1

    Article  CAS  Google Scholar 

  34. Garland DE, Adkins RH, Scott M, Singh H, Massih M, Stewart C (2004) Bone loss at the os calcis compared with bone loss at the knee in individuals with spinal cord injury. J Spinal Cord Med 27(3):207–211

    Article  PubMed  Google Scholar 

  35. Garland DE, Adkins RH, Stewart CA (2008) Five-year longitudinal bone evaluations in individuals with chronic complete spinal cord injury. The journal of spinal cord medicine 31(5):543–550

    Article  PubMed  PubMed Central  Google Scholar 

  36. Baim S, Wilson CR, Lewiecki EM, Luckey MM, Downs RW Jr, Lentle BC (2005) Precision assessment and radiation safety for dual-energy X-ray absorptiometry: position paper of the International Society for Clinical Densitometry. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 8(4):371–378

    Article  Google Scholar 

  37. Diez-Perez A, Adachi JD, Agnusdei D, Bilezikian JP, Compston JE, Cummings SR, Eastell R, Eriksen EF, Gonzalez-Macias J, Liberman UA, Wahl DA, Seeman E, Kanis JA, Cooper C, Group ICIRW (2012) Treatment failure in osteoporosis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 23(12):2769–2774. doi:10.1007/s00198-012-2093-8

    Article  CAS  Google Scholar 

  38. Murphy E, Bresnihan B, FitzGerald O (2001) Validated measurement of periarticular bone mineral density at the knee joint by dual energy x ray absorptiometry. Ann Rheum Dis 60(1):8–13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Bohr HH, Schaadt O (1987) Mineral content of upper tibia assessed by dual photon densitometry. Acta Orthop Scand 58(5):557–559

    Article  PubMed  CAS  Google Scholar 

  40. Li MG, Nilsson KG, Nivbrant B (2004) Decreased precision for BMD measurements in the prosthetic knee using a non-knee-specific software. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 7(3):319–325

    Article  Google Scholar 

  41. McPherson JG, Edwards WB, Prasad A, Troy KL, Griffith JW, Schnitzer TJ (2014) Dual energy X-ray absorptiometry of the knee in spinal cord injury: methodology and correlation with quantitative computed tomography. Spinal Cord 52(11):821–825. doi:10.1038/sc.2014.122

    Article  PubMed  CAS  Google Scholar 

  42. Forrest G, Harkema S, Angeli C, Faghri P, Kirshblum S, Cirnigliaro C, Garbarinin E, Bauman W (2013) Preliminary results on the differential effect on bone of applying multi-muscle electrical stimulation to the leg while supine or standing in patients with SCI: the importance of combining a mechanical intervention with gravitational loading. J Spinal Cord Med Accepted for Publication

  43. Bauman W, Cirnigliaro C, LaFountaine M, Martinez L, Kirshblum S, Spungen A (2014) Zoledronic acid administration failed to prevent bone loss at the knee in persons with acute spinal cord injury: an observational cohort study. J Bone Miner Metab Accepted for Publication

  44. Bakkum AJ, Janssen TW, Rolf MP, Roos JC, Burcksen J, Knol DL, de Groot S (2014) A reliable method for measuring proximal tibia and distal femur bone mineral density using dual-energy X-ray absorptiometry. Med Eng Phys 36(3):387–390. doi:10.1016/j.medengphy.2013.08.010

    Article  PubMed  Google Scholar 

  45. Gilchrist N, Hooper G, Frampton C, Maguire P, Heard A, March RL, Maxwell R, Penny I (2013) Measurement of bone density around the Oxford medial compartment knee replacement using iDXA. A precision study. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 16(2):178–182. doi:10.1016/j.jocd.2012.02.015

    Article  Google Scholar 

  46. Morse LR, Lazzari AA, Battaglino R, Stolzmann KL, Matthess KR, Gagnon DR, Davis SA, Garshick E (2009) Dual energy x-ray absorptiometry of the distal femur may be more reliable than the proximal tibia in spinal cord injury. Arch Phys Med Rehabil 90(5):827–831. doi:10.1016/j.apmr.2008.12.004

    Article  PubMed  PubMed Central  Google Scholar 

  47. Bauman WA, Cirnigliaro CM, La Fountaine MF, Martinez L, Kirshblum SC, Spungen AM (2014) Zoledronic acid administration failed to prevent bone loss at the knee in persons with acute spinal cord injury: an observational cohort study. J Bone Miner Metab. doi:10.1007/s00774-014-0602-x

    Article  PubMed  Google Scholar 

  48. Schnitzer TJ, Kim K, Marks J, Yeasted R, Simonian N, Chen D (2016) Zoledronic acid treatment after acute spinal cord injury: results of a randomized, placebo-controlled pilot trial. PM & R: the journal of injury, function, and rehabilitation. doi:10.1016/j.pmrj.2016.01.012

    Article  Google Scholar 

  49. Lauer R, Johnston TE, Smith BT, Mulcahey MJ, Betz RR, Maurer AH (2007) Bone mineral density of the hip and knee in children with spinal cord injury. J Spinal cord Med 30(Suppl 1):S10–S14

    Article  PubMed  PubMed Central  Google Scholar 

  50. Prentice A, Parsons TJ, Cole TJ (1994) Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants. Am J Clin Nutr 60(6):837–842

    Article  PubMed  CAS  Google Scholar 

  51. Tothill P, Avenell A, Reid DM (1994) Precision and accuracy of measurements of whole-body bone mineral: comparisons between Hologic, Lunar and Norland dual-energy X-ray absorptiometers. Br J Radiol 67(804):1210–1217. doi:10.1259/0007-1285-67-804-1210

    Article  PubMed  CAS  Google Scholar 

  52. Pors Nielsen S, Barenholdt O, Diessel E, Armbrust S, Felsenberg D (1998) Linearity and accuracy errors in bone densitometry. Br J Radiol 71(850):1062–1068. doi:10.1259/bjr.71.850.10211067

    Article  PubMed  CAS  Google Scholar 

  53. Craven R, McGillivray A (2009) Detection and treatment of sublesional osteoporosis among patients with chronic spinal cord injury. Topics in spinal cord injury rehabilitation 14(4):1–22. doi:10.1310/sci1404-1

    Article  Google Scholar 

  54. Rittweger J, Goosey-Tolfrey VL, Cointry G, Ferretti JL (2010) Structural analysis of the human tibia in men with spinal cord injury by tomographic (pQCT) serial scans. Bone 47(3):511–518. doi:10.1016/j.bone.2010.05.025

    Article  PubMed  Google Scholar 

  55. Coupaud S, McLean AN, Purcell M, Fraser MH, Allan DB (2015) Decreases in bone mineral density at cortical and trabecular sites in the tibia and femur during the first year of spinal cord injury. Bone 74:69–75. doi:10.1016/j.bone.2015.01.005

    Article  PubMed  Google Scholar 

  56. Burghardt AJ, Link TM, Majumdar S (2011) High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res 469(8):2179–2193. doi:10.1007/s11999-010-1766-x

    Article  PubMed  PubMed Central  Google Scholar 

  57. Ito M, Ikeda K, Nishiguchi M, Shindo H, Uetani M, Hosoi T, Orimo H (2005) Multi-detector row CT imaging of vertebral microstructure for evaluation of fracture risk. J Bone Miner Res Off J Am Soc Bone Miner Res 20(10):1828–1836. doi:10.1359/JBMR.050610

    Article  Google Scholar 

  58. Lee SY, Kwon SS, Kim HS, Yoo JH, Kim J, Kim JY, Min BC, Moon SJ, Sung KH (2015) Reliability and validity of lower extremity computed tomography as a screening tool for osteoporosis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 26(4):1387–1394. doi:10.1007/s00198-014-3013-x

    Article  CAS  Google Scholar 

  59. Giangregorio LM, Gibbs JC, Craven BC (2016) Measuring muscle and bone in individuals with neurologic impairment; lessons learned about participant selection and pQCT scan acquisition and analysis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 27(8):2433–2446. doi:10.1007/s00198-016-3572-0

    Article  CAS  Google Scholar 

  60. Engelke K, Lang T, Khosla S, Qin L, Zysset P, Leslie WD, Shepherd JA, Schousboe JT (2015) Clinical use of quantitative computed tomography (QCT) of the hip in the management of osteoporosis in adults: the 2015 ISCD official positions—part I. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 18(3):338–358. doi:10.1016/j.jocd.2015.06.012

    Article  Google Scholar 

  61. Cervinka T, Sievanen H, Hyttinen J, Rittweger J (2014) Bone loss patterns in cortical, subcortical, and trabecular compartments during simulated microgravity. J Appl Physiol 117(1):80–88. doi:10.1152/japplphysiol.00021.2014

    Article  PubMed  Google Scholar 

  62. Dudley-Javoroski S, Amelon R, Liu Y, Saha PK, Shields RK (2014) High bone density masks architectural deficiencies in an individual with spinal cord injury. J Spinal cord Med 37(3):349–354. doi:10.1179/2045772313Y.0000000166

    Article  PubMed  PubMed Central  Google Scholar 

  63. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res Off J Am Soc Bone Miner Res 25(7):1468–1486. doi:10.1002/jbmr.141

    Article  Google Scholar 

  64. Krug R, Burghardt AJ, Majumdar S, Link TM (2010) High-resolution imaging techniques for the assessment of osteoporosis. Radiol Clin N Am 48(3):601–621. doi:10.1016/j.rcl.2010.02.015

    Article  PubMed  Google Scholar 

  65. Dudley-Javoroski S, Shields RK (2012) Regional cortical and trabecular bone loss after spinal cord injury. J Rehabil Res Dev 49(9):1365–1376

    Article  PubMed  PubMed Central  Google Scholar 

  66. Coupaud S, McLean AN, Allan DB (2009) Role of peripheral quantitative computed tomography in identifying disuse osteoporosis in paraplegia. Skelet Radiol 38(10):989–995. doi:10.1007/s00256-009-0674-1

    Article  Google Scholar 

  67. Frotzler A, Cheikh-Sarraf B, Pourtehrani M, Krebs J, Lippuner K (2015) Long-bone fractures in persons with spinal cord injury. Spinal Cord 53(9):701–704. doi:10.1038/sc.2015.74

    Article  PubMed  CAS  Google Scholar 

  68. Pop LC, Sukumar D, Tomaino K, Schlussel Y, Schneider SH, Gordon CL, Wang X, Shapses SA (2015) Moderate weight loss in obese and overweight men preserves bone quality. Am J Clin Nutr 101(3):659–667. doi:10.3945/ajcn.114.088534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Giangregorio L, Lala D, Hummel K, Gordon C, Craven BC (2013) Measuring apparent trabecular density and bone structure using peripheral quantitative computed tomography at the tibia: precision in participants with and without spinal cord injury. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 16(2):139–146. doi:10.1016/j.jocd.2012.02.003

    Article  Google Scholar 

  70. Edwards WB, Schnitzer TJ, Troy KL (2014) The mechanical consequence of actual bone loss and simulated bone recovery in acute spinal cord injury. Bone 60:141–147. doi:10.1016/j.bone.2013.12.012

    Article  PubMed  Google Scholar 

  71. Rajapakse CS, Magland J, Zhang XH, Liu XS, Wehrli SL, Guo XE, Wehrli FW (2009) Implications of noise and resolution on mechanical properties of trabecular bone estimated by image-based finite-element analysis. Journal of orthopaedic research: official publication of the Orthopaedic Research Society 27(10):1263–1271. doi:10.1002/jor.20877

    Article  Google Scholar 

  72. Wehrli FW, Gomberg BR, Saha PK, Song HK, Hwang SN, Snyder PJ (2001) Digital topological analysis of in vivo magnetic resonance microimages of trabecular bone reveals structural implications of osteoporosis. J Bone Miner Res Off J Am Soc Bone Miner Res 16(8):1520–1531. doi:10.1359/jbmr.2001.16.8.1520

    Article  CAS  Google Scholar 

  73. Chesnut CH 3rd, Majumdar S, Newitt DC, Shields A, Van Pelt J, Laschansky E, Azria M, Kriegman A, Olson M, Eriksen EF, Mindeholm L (2005) Effects of salmon calcitonin on trabecular microarchitecture as determined by magnetic resonance imaging: results from the QUEST study. J Bone Miner Res Off J Am Soc Bone Miner Res 20(9):1548–1561. doi:10.1359/JBMR.050411

    Article  CAS  Google Scholar 

  74. Slade JM, Bickel CS, Modlesky CM, Majumdar S, Dudley GA (2005) Trabecular bone is more deteriorated in spinal cord injured versus estrogen-free postmenopausal women. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 16(3):263–272. doi:10.1007/s00198-004-1665-7

    Article  Google Scholar 

  75. Lazo MG, Shirazi P, Sam M, Giobbie-Hurder A, Blacconiere MJ, Muppidi M (2001) Osteoporosis and risk of fracture in men with spinal cord injury. Spinal Cord 39(4):208–214. doi:10.1038/sj.sc.3101139

    Article  PubMed  CAS  Google Scholar 

  76. Vestergaard P, Krogh K, Rejnmark L, Mosekilde L (1998) Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord 36(11):790–796

    Article  PubMed  CAS  Google Scholar 

  77. Parsons KC, Lammertse DP (1991) Rehabilitation in spinal cord disorders. 1. Epidemiology, prevention, and system of care of spinal cord disorders. Arch Phys Med Rehabil 72(4-S):S293–S294

    PubMed  CAS  Google Scholar 

  78. Freehafer AA (1995) Limb fractures in patients with spinal cord injury. Arch Phys Med Rehabil 76(9):823–827

    Article  PubMed  CAS  Google Scholar 

  79. Garland DE, Adkins RH, Kushwaha V, Stewart C (2004) Risk factors for osteoporosis at the knee in the spinal cord injury population. J Spinal Cord Med 27(3):202–206

    Article  PubMed  Google Scholar 

  80. Martinez A, Cuenca J, Herrera A, Domingo J (2002) Late lower extremity fractures in patients with paraplegia. Injury 33(7):583–586

    Article  PubMed  Google Scholar 

  81. Gifre L, Vidal J, Carrasco J, Portell E, Puig J, Monegal A, Guanabens N, Peris P (2014) Incidence of skeletal fractures after traumatic spinal cord injury: a 10-year follow-up study. Clin Rehabil 28(4):361–369. doi:10.1177/0269215513501905

    Article  PubMed  Google Scholar 

  82. Comarr AE, Hutchinson RH, Bors E (1962) Extremity fractures of patients with spinal cord injuries. Am J Surg 103:732–739

    Article  PubMed  CAS  Google Scholar 

  83. Zehnder Y, Luthi M, Michel D, Knecht H, Perrelet R, Neto I, Kraenzlin M, Zach G, Lippuner K (2004) Long-term changes in bone metabolism, bone mineral density, quantitative ultrasound parameters, and fracture incidence after spinal cord injury: a cross-sectional observational study in 100 paraplegic men. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 15(3):180–189. doi:10.1007/s00198-003-1529-6

    Article  Google Scholar 

  84. Freehafer AA, Mast WA (1965) Lower extremity fractures in patients with spinal-cord injury. J Bone Joint Surg Am 47:683–694

    Article  PubMed  CAS  Google Scholar 

  85. Garland DE, Maric Z, Adkins RH, Stewart CA (1993) Bone mineral density about the knee in spinal cord injured patients with pathologic fractures. Contemp Orthop 26:375–379

  86. Mazess RB (1990) Bone densitometry of the axial skeleton. Orthopedic Clinic North Am 21(1):51–63

    CAS  Google Scholar 

  87. Eser P, Frotzler A, Zehnder Y, Denoth J (2005) Fracture threshold in the femur and tibia of people with spinal cord injury as determined by peripheral quantitative computed tomography. Arch Phys Med Rehabil 86(3):498–504. doi:10.1016/j.apmr.2004.09.006

    Article  PubMed  Google Scholar 

  88. Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporosis and the bone mass effects of mechanical and nonmechanical agents. Bone Min 2(2):73–85

    CAS  Google Scholar 

  89. Isaacson J, Brotto M (2014) Physiology of mechanotransduction: how do muscle and bone “talk” to one another? Clin Rev Bone Min metab 12(2):77–85. doi:10.1007/s12018-013-9152-3

    Article  Google Scholar 

  90. Dolbow DR, Gorgey AS, Gater DR, Moore JR (2014) Body composition changes after 12 months of FES cycling: case report of a 60-year-old female with paraplegia. Spinal Cord 52(Suppl 1):S3–S4. doi:10.1038/sc.2014.40

    Article  PubMed  Google Scholar 

  91. Pacy PJ, Hesp R, Halliday DA, Katz D, Cameron G, Reeve J (1988) Muscle and bone in paraplegic patients, and the effect of functional electrical stimulation. Clin Sci 75(5):481–487

    Article  PubMed  CAS  Google Scholar 

  92. Biering-Sorensen F, Hansen B, Lee BS (2009) Non-pharmacological treatment and prevention of bone loss after spinal cord injury: a systematic review. Spinal Cord 47(7):508–518. doi:10.1038/sc.2008.177

    Article  PubMed  CAS  Google Scholar 

  93. Guertin PA (2009) Recovery of locomotor function with combinatory drug treatments designed to synergistically activate specific neuronal networks. Curr Med Chem 16(11):1366–1371

    Article  PubMed  CAS  Google Scholar 

  94. de Bruin ED, Frey-Rindova P, Herzog RE, Dietz V, Dambacher MA, Stussi E (1999) Changes of tibia bone properties after spinal cord injury: effects of early intervention. Arch Phys Med Rehabil 80(2):214–220

    Article  PubMed  Google Scholar 

  95. Giangregorio LM, Hicks AL, Webber CE, Phillips SM, Craven BC, Bugaresti JM, McCartney N (2005) Body weight supported treadmill training in acute spinal cord injury: impact on muscle and bone. Spinal Cord 43(11):649–657. doi:10.1038/sj.sc.3101774

    Article  PubMed  CAS  Google Scholar 

  96. Bloomfield SA, Mysiw WJ, Jackson RD (1996) Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone 19(1):61–68

    Article  PubMed  CAS  Google Scholar 

  97. Frotzler A, Coupaud S, Perret C, Kakebeeke TH, Hunt KJ, Donaldson Nde N, Eser P (2008) High-volume FES-cycling partially reverses bone loss in people with chronic spinal cord injury. Bone 43(1):169–176. doi:10.1016/j.bone.2008.03.004

    Article  PubMed  Google Scholar 

  98. Lai CH, Chang WH, Chan WP, Peng CW, Shen LK, Chen JJ, Chen SC (2010) Effects of functional electrical stimulation cycling exercise on bone mineral density loss in the early stages of spinal cord injury. J Rehabil Med 42(2):150–154. doi:10.2340/16501977-0499

    Article  PubMed  Google Scholar 

  99. Eser P, de Bruin ED, Telley I, Lechner HE, Knecht H, Stussi E (2003) Effect of electrical stimulation-induced cycling on bone mineral density in spinal cord-injured patients. Eur J Clin Investig 33(5):412–419

    Article  CAS  Google Scholar 

  100. Dudley-Javoroski S, Saha PK, Liang G, Li C, Gao Z, Shields RK (2012) High dose compressive loads attenuate bone mineral loss in humans with spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 23(9):2335–2346. doi:10.1007/s00198-011-1879-4

    Article  CAS  Google Scholar 

  101. Belanger M, Stein RB, Wheeler GD, Gordon T, Leduc B (2000) Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil 81(8):1090–1098

    Article  PubMed  CAS  Google Scholar 

  102. Chen SC, Lai CH, Chan WP, Huang MH, Tsai HW, Chen JJ (2005) Increases in bone mineral density after functional electrical stimulation cycling exercises in spinal cord injured patients. Disabil Rehabil 27(22):1337–1341. doi:10.1080/09638280500164032

    Article  PubMed  Google Scholar 

  103. Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M (1997) Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int 61(1):22–25

    Article  PubMed  CAS  Google Scholar 

  104. Shields RK, Dudley-Javoroski S (2007) Musculoskeletal adaptations in chronic spinal cord injury: effects of long-term soleus electrical stimulation training. Neurorehabil Neural Repair 21(2):169–179. doi:10.1177/1545968306293447

    Article  PubMed  PubMed Central  Google Scholar 

  105. Dudley-Javoroski S, Shields RK (2013) Active-resisted stance modulates regional bone mineral density in humans with spinal cord injury. J spinal cord Med 36(3):191–199. doi:10.1179/2045772313Y.0000000092

    Article  PubMed  PubMed Central  Google Scholar 

  106. Forrest G, Harkema SJ, Angeli CA, Faghri PD, Kirshblum SC, Cirnigliaro CM, LaFountaine, Garbarini E, Bauman WA. (2014) Preliminary results on the differential effect on bone of applying multi-muscle electrical stimulation to the leg while supine or standing in patients with SCI: the importance of combining a mechanical intervention with gravitational loading. The journal of spinal cord medicine In Preparation

  107. Ben M, Harvey L, Denis S, Glinsky J, Goehl G, Chee S, Herbert RD (2005) Does 12 weeks of regular standing prevent loss of ankle mobility and bone mineral density in people with recent spinal cord injuries? Australian J physiother 51(4):251–256

    Article  Google Scholar 

  108. Warden SJ, Bennell KL, Matthews B, Brown DJ, McMeeken JM, Wark JD (2001) Efficacy of low-intensity pulsed ultrasound in the prevention of osteoporosis following spinal cord injury. Bone 29(5):431–436

    Article  PubMed  CAS  Google Scholar 

  109. Wuermser LA, Beck LA, Lamb JL, Atkinson EJ, Amin S (2014) The effect of low-magnitude whole body vibration on bone density and microstructure in men and women with chronic motor complete paraplegia. J Spinal cord Med. doi:10.1179/2045772313Y.0000000191

    Article  PubMed Central  PubMed  Google Scholar 

  110. Bultink IE, Baden M, Lems WF (2013) Glucocorticoid-induced osteoporosis: an update on current pharmacotherapy and future directions. Expert Opin Pharmacother 14(2):185–197. doi:10.1517/14656566.2013.761975

    Article  PubMed  CAS  Google Scholar 

  111. Chappard D, Minaire P, Privat C, Berard E, Mendoza-Sarmiento J, Tournebise H, Basle MF, Audran M, Rebel A, Picot C et al (1995) Effects of tiludronate on bone loss in paraplegic patients. J Bone Miner Res Off J Am Soc Bone Miner Res 10(1):112–118. doi:10.1002/jbmr.5650100116

    Article  CAS  Google Scholar 

  112. Pearson EG, Nance PW, Leslie WD, Ludwig S (1997) Cyclical etidronate: its effect on bone density in patients with acute spinal cord injury. Arch Phys Med Rehabil 78(3):269–272

    Article  PubMed  CAS  Google Scholar 

  113. Nance PW, Schryvers O, Leslie W, Ludwig S, Krahn J, Uebelhart D (1999) Intravenous pamidronate attenuates bone density loss after acute spinal cord injury. Arch Phys Med Rehabil 80(3):243–251

    Article  PubMed  CAS  Google Scholar 

  114. Gilchrist NL, Frampton CM, Acland RH, Nicholls MG, March RL, Maguire P, Heard A, Reilly P, Marshall K (2007) Alendronate prevents bone loss in patients with acute spinal cord injury: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab 92(4):1385–1390. doi:10.1210/jc.2006-2013

    Article  PubMed  CAS  Google Scholar 

  115. Bauman WA, Wecht JM, Kirshblum S, Spungen AM, Morrison N, Cirnigliaro C, Schwartz E (2005) Effect of pamidronate administration on bone in patients with acute spinal cord injury. J Rehabil Res Dev 42(3):305–313

    Article  PubMed  Google Scholar 

  116. Bubbear JS, Gall A, Middleton FR, Ferguson-Pell M, Swaminathan R, Keen RW (2011) Early treatment with zoledronic acid prevents bone loss at the hip following acute spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 22(1):271–279. doi:10.1007/s00198-010-1221-6

    Article  CAS  Google Scholar 

  117. Shapiro J, Smith B, Beck T, Ballard P, Dapthary M, BrintzenhofeSzoc K, Caminis J (2007) Treatment with zoledronic acid ameliorates negative geometric changes in the proximal femur following acute spinal cord injury. Calcif Tissue Int 80(5):316–322. doi:10.1007/s00223-007-9012-6

    Article  PubMed  CAS  Google Scholar 

  118. Gifre L, Vidal J, Carrasco JL, Muxi A, Portell E, Monegal A, Guanabens N, Peris P (2016) Denosumab increases sublesional bone mass in osteoporotic individuals with recent spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 27(1):405–410. doi:10.1007/s00198-015-3333-5

    Article  CAS  Google Scholar 

  119. Schousboe JT (2014) ISCD in 2014: state of the society. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 17(3):328–329. doi:10.1016/j.jocd.2014.04.118

    Article  Google Scholar 

  120. Krueger D (2015) ISCD in 2015: state of the society. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 18(3):445–446. doi:10.1016/j.jocd.2015.06.004

    Article  Google Scholar 

  121. Qin W, Li X, Peng Y, Harlow LM, Ren Y, Wu Y, Li J, Qin Y, Sun J, Zheng S, Brown T, Feng JQ, Ke HZ, Bauman WA, Cardozo CP (2015) Sclerostin Antibody Preserves the Morphology and Structure of Osteocytes and Blocks the Severe Skeletal Deterioration After Motor-Complete Spinal Cord Injury in Rats. J Bone Miner Res 30(11):1994–2004

  122. Qin W, Zhao W, Li X, Peng Y, Harlow LM, Li J, Qin Y, Pan J, Wu Y, Ran L, Ke HZ, Cardozo CP, Bauman WA. Mice with sclerostin gene deletion are resistant to the severe sublesional bone loss induced by spinal cord injury. Osteoporos Int. 2016 20. [Epub ahead of print])

  123. Battaglino RA, Sudhakar S, Lazzari AA, Garshick E, Zafonte R, Morse LR (2012) Circulating sclerostin is elevated in short-term and reduced in long-term SCI. Bone 51(3):600–605. doi:10.1016/j.bone.2012.04.019

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Doherty AL, Battaglino RA, Donovan J, Gagnon D, Lazzari AA, Garshick E, Zafonte R, Morse LR (2014) Adiponectin is a candidate biomarker of lower extremity bone density in men with chronic spinal cord injury. J Bone Miner Res Off J Am Soc Bone Miner Res 29(1):251–259. doi:10.1002/jbmr.2020

    Article  CAS  Google Scholar 

  125. Moreno C (2001) Protocol for using dual photon absorptiometry software to measure BMD of distal femur and proximal tibia. Master’s thesis, McMaster University, Hamilton

    Google Scholar 

  126. Morse LR, Sudhakar S, Danilack V, Tun C, Lazzari A, Gagnon DR, Garshick E, Battaglino RA (2012) Association between sclerostin and bone density in chronic spinal cord injury. J Bone Miner Res Off J Am Soc Bone Miner Res 27(2):352–359. doi:10.1002/jbmr.546

    Article  CAS  Google Scholar 

  127. Morse LR, Sudhakar S, Lazzari AA, Tun C, Garshick E, Zafonte R, Battaglino RA (2013) Sclerostin: a candidate biomarker of SCI-induced osteoporosis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 24(3):961–968. doi:10.1007/s00198-012-2072-0

    Article  CAS  Google Scholar 

  128. McCarthy ID, Bloomer Z, Gall A, Keen R, Ferguson-Pell M (2012) Changes in the structural and material properties of the tibia in patients with spinal cord injury. Spinal Cord 50(4):333–337. doi:10.1038/sc.2011.143

    Article  PubMed  CAS  Google Scholar 

  129. Tan CO, Battaglino RA, Doherty AL, Gupta R, Lazzari AA, Garshick E, Zafonte R, Morse LR (2014) Adiponectin is associated with bone strength and fracture history in paralyzed men with spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 25(11):2599–2607. doi:10.1007/s00198-014-2786-2

    Article  CAS  Google Scholar 

  130. Dudley-Javoroski S, Shields RK (2010) Longitudinal changes in femur bone mineral density after spinal cord injury: effects of slice placement and peel method. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 21(6):985–995. doi:10.1007/s00198-009-1044-5

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank the James J. Peters Veterans Affairs Medical Center, Bronx, NY, the Department of Veterans Affairs Rehabilitation Research & Development Service, and the Kessler Institute for Rehabilitation, West Orange, NJ, for their support to perform this work. The authors would also like to thank the Department of Physical Therapy, School of Health Related Professions, Rutgers New Jersey Medical School, Newark, NJ, USA and Alex T. Lombard for his assistance completing the comprehensive literature review necessary to complete this review article.

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Authors and Affiliations

  1. Department of Veterans Affairs Rehabilitation Research & Development Service National Center for the Medical Consequences of Spinal Cord Injury, James J. Peters Veterans Affairs Medical Center, Bronx, NY, USA

    C. M. Cirnigliaro, M. F. La Fountaine & W. A. Bauman

  2. Department of Physical Therapy, School of Health Related Professions, Rutgers New Jersey Medical School, Newark, NJ, USA

    M. J. Myslinski

  3. Department of Physical Therapy, School of Health and Medical Sciences, Seton Hall University, South Orange, NJ, USA

    M. F. La Fountaine

  4. The Institute for Advanced Study of Rehabilitation and Sports Science, School of Health and Medical Sciences, Seton Hall University, South Orange, NJ, USA

    M. F. La Fountaine

  5. Kessler Institute for Rehabilitation, West Orange, NJ, USA

    S. C. Kirshblum

  6. Department of Physical Medicine and Rehabilitation, Rutgers New Jersey Medical School, Newark, NJ, USA

    S. C. Kirshblum & G. F. Forrest

  7. Kessler Foundation, West Orange, NJ, USA

    G. F. Forrest

  8. Departments of Medicine and Rehabilitation Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    W. A. Bauman

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  1. C. M. Cirnigliaro
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  3. M. F. La Fountaine
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  4. S. C. Kirshblum
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Correspondence to W. A. Bauman.

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Veterans Affairs Rehabilitation Research and Development Service (#B9212-C, B2020-C) and the James J. Peters VA Medical Center.

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Cirnigliaro, C.M., Myslinski, M.J., La Fountaine, M.F. et al. Bone loss at the distal femur and proximal tibia in persons with spinal cord injury: imaging approaches, risk of fracture, and potential treatment options. Osteoporos Int 28, 747–765 (2017). https://doi.org/10.1007/s00198-016-3798-x

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