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Predictive ability of heel quantitative ultrasound for incident fractures: an individual-level meta-analysis

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Abstract

Summary

The relationship between bone quantitative ultrasound (QUS) and fracture risk was estimated in an individual level data meta-analysis of 9 prospective studies of 46,124 individuals and 3018 incident fractures. Low QUS is associated with an increase in fracture risk, including hip fracture. The association with osteoporotic fracture decreases with time.

Introduction

The aim of this meta-analysis was to investigate the association between parameters of QUS and risk of fracture.

Methods

In an individual-level analysis, we studied participants in nine prospective cohorts from Asia, Europe and North America. Heel broadband ultrasonic attenuation (BUA dB/MHz) and speed of sound (SOS m/s) were measured at baseline. Fractures during follow-up were collected by self-report and in some cohorts confirmed by radiography. An extension of Poisson regression was used to examine the gradient of risk (GR, hazard ratio per 1 SD decrease) between QUS and fracture risk adjusted for age and time since baseline in each cohort. Interactions between QUS and age and time since baseline were explored.

Results

Baseline measurements were available in 46,124 men and women, mean age 70 years (range 20–100). Three thousand and eighteen osteoporotic fractures (787 hip fractures) occurred during follow-up of 214,000 person-years. The summary GR for osteoporotic fracture was similar for both BUA (1.45, 95 % confidence intervals (CI) 1.40–1.51) and SOS (1.42, 95 % CI 1.36–1.47). For hip fracture, the respective GRs were 1.69 (95 % CI, 1.56–1.82) and 1.60 (95 % CI, 1.48–1.72). However, the GR was significantly higher for both fracture outcomes at lower baseline BUA and SOS (p < 0.001). The predictive value of QUS was the same for men and women and for all ages (p > 0.20), but the predictive value of both BUA and SOS for osteoporotic fracture decreased with time (p = 0.018 and p = 0.010, respectively). For example, the GR of BUA for osteoporotic fracture, adjusted for age, was 1.51 (95 % CI 1.42–1.61) at 1 year after baseline, but at 5 years, it was 1.36 (95 % CI 1.27–1.46).

Conclusions

Our results confirm that quantitative ultrasound is an independent predictor of fracture for men and women particularly at low QUS values.

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References

  1. Kanis JA (2008) On behalf of the WHO scientific group. Assessment of osteoporosis at the primary health-care level. Technical report. WHO Collaborating Centre, University of Sheffield, UK, Sheffield

    Google Scholar 

  2. Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359(9321):1929–1936

    Article  PubMed  Google Scholar 

  3. Kanis JA, Borgstrom F, De Laet C et al (2005) Assessment of fracture risk. Osteoporos Int 16(6):581–589

    Article  PubMed  Google Scholar 

  4. Kanis JA, Johnell O, Oden A, Johansson H, McCloskey E (2008) FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int 19(4):385–397

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Kanis JA, McCloskey EV, Johansson H, Oden A, Melton LJ 3rd, Khaltaev N (2008) A reference standard for the description of osteoporosis. Bone 42(3):467–475

    Article  CAS  PubMed  Google Scholar 

  6. Hernlund E, Svedbom A, Ivergard M et al (2013) Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 8(1–2):136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Bauer DC, Ewing SK, Cauley JA, Ensrud KE, Cummings SR, Orwoll ES (2007) Quantitative ultrasound predicts hip and non-spine fracture in men: the MrOS study. Osteoporos Int 18(6):771–777

    Article  CAS  PubMed  Google Scholar 

  8. Bauer DC, Gluer CC, Cauley JA et al (1997) Broadband ultrasound attenuation predicts fractures strongly and independently of densitometry in older women. A prospective study. Study of osteoporotic fractures research group. Arch Intern Med 157(6):629–634

    Article  CAS  PubMed  Google Scholar 

  9. Dargent-Molina P, Schott AM, Hans D et al (1999) Separate and combined value of bone mass and gait speed measurements in screening for hip fracture risk: results from the EPIDOS study. Epidemiologie de l’Osteoporose. Osteoporos Int 9(2):188–192

    Article  CAS  PubMed  Google Scholar 

  10. Diez-Perez A, Gonzalez-Macias J, Marin F et al (2007) Prediction of absolute risk of non-spinal fractures using clinical risk factors and heel quantitative ultrasound. Osteoporos Int 18(5):629–639

    Article  CAS  PubMed  Google Scholar 

  11. Fujiwara S, Sone T, Yamazaki K et al (2005) Heel bone ultrasound predicts non-spine fracture in Japanese men and women. Osteoporos Int 16(12):2107–2112

    Article  CAS  PubMed  Google Scholar 

  12. Gnudi S, Ripamonti C, Malavolta N (2000) Quantitative ultrasound and bone densitometry to evaluate the risk of nonspine fractures: a prospective study. Osteoporos Int 11(6):518–523

    Article  CAS  PubMed  Google Scholar 

  13. Hans D, Dargent-Molina P, Schott AM et al (1996) Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study. Lancet 348(9026):511–514

    Article  CAS  PubMed  Google Scholar 

  14. Hollaender R, Hartl F, Krieg MA et al (2009) Prospective evaluation of risk of vertebral fractures using quantitative ultrasound measurements and bone mineral density in a population-based sample of postmenopausal women: results of the Basel Osteoporosis Study. Ann Rheum Dis 68(3):391–396

    Article  CAS  PubMed  Google Scholar 

  15. Huang C, Ross PD, Yates AJ et al (1998) Prediction of fracture risk by radiographic absorptiometry and quantitative ultrasound: a prospective study. Calcif Tissue Int 63(5):380–384

    Article  CAS  PubMed  Google Scholar 

  16. Khaw KT, Reeve J, Luben R et al (2004) Prediction of total and hip fracture risk in men and women by quantitative ultrasound of the calcaneus: EPIC-Norfolk prospective population study. Lancet 363(9404):197–202

    Article  PubMed  Google Scholar 

  17. Krieg MA, Cornuz J, Ruffieux C et al (2006) Prediction of hip fracture risk by quantitative ultrasound in more than 7000 Swiss women > or =70 years of age: comparison of three technologically different bone ultrasound devices in the SEMOF study. J Bone Miner Res 21(9):1457–1463

    Article  PubMed  Google Scholar 

  18. Marin F, Gonzalez-Macias J, Diez-Perez A, Palma S, Delgado-Rodriguez M (2006) Relationship between bone quantitative ultrasound and fractures: a meta-analysis. J Bone Miner Res 21(7):1126–1135

    Article  PubMed  Google Scholar 

  19. Moayyeri A, Adams JE, Adler RA et al (2012) Quantitative ultrasound of the heel and fracture risk assessment: an updated meta-analysis. Osteoporos Int 23(1):143–153

    Article  CAS  PubMed  Google Scholar 

  20. Pinheiro MM, Castro CM, Szejnfeld VL (2006) Low femoral bone mineral density and quantitative ultrasound are risk factors for new osteoporotic fracture and total and cardiovascular mortality: a 5-year population-based study of Brazilian elderly women. J Gerontol A Biol Sci Med Sci 61(2):196–203

    Article  PubMed  Google Scholar 

  21. Stewart A, Kumar V, Reid DM (2006) Long-term fracture prediction by DXA and QUS: a 10-year prospective study. J Bone Miner Res 21(3):413–418

    Article  PubMed  Google Scholar 

  22. Schousboe JT, Shepherd JA, Bilezikian JP, Baim S (2013) Executive summary of the 2013 international society for clinical densitometry position development conference on bone densitometry. J Clin Densitom 16(4):455–466

    Article  PubMed  Google Scholar 

  23. Heaney RP, Kanis JA (1996) The interpretation and utility of ultrasound measurements of bone. Bone 18(6):491–492

    Article  CAS  PubMed  Google Scholar 

  24. Gluer CC (1997) Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. The international quantitative ultrasound consensus group. J Bone Miner Res 12(8):1280–1288

    Article  CAS  PubMed  Google Scholar 

  25. Gluer CC, Barkmann R (2003) Quantitative ultrasound: use in the detection of fractures and in the assessment of bone composition. Curr Osteoporos Rep 1(3):98–104

    Article  PubMed  Google Scholar 

  26. Hans D, Krieg MA (2008) The clinical use of quantitative ultrasound (QUS) in the detection and management of osteoporosis. IEEE Trans Ultrason Ferroelectr Freq Control 55(7):1529–1538

    Article  CAS  PubMed  Google Scholar 

  27. Hans D, Durosier C, Kanis JA, Johansson H, Schott-Pethelaz AM, Krieg MA (2008) Assessment of the 10-year probability of osteoporotic hip fracture combining clinical risk factors and heel bone ultrasound: The EPISEM Prospective Cohort of 12958 Elderly Women. J Bone Miner Res

  28. Schott AM, Cormier C, Hans D et al (1998) How hip and whole-body bone mineral density predict hip fracture in elderly women: the EPIDOS Prospective Study. Osteoporos Int 8(3):247–254

    Article  CAS  PubMed  Google Scholar 

  29. Lunt M, Felsenberg D, Adams J et al (1997) Population-based geographic variations in DXA bone density in Europe: the EVOS Study. European Vertebral Osteoporosis. Osteoporos Int 7(3):175–189

    Article  CAS  PubMed  Google Scholar 

  30. Lunt M, Felsenberg D, Reeve J et al (1997) Bone density variation and its effects on risk of vertebral deformity in men and women studied in thirteen European centers: the EVOS Study. J Bone Miner Res 12(11):1883–1894

    Article  CAS  PubMed  Google Scholar 

  31. O’Neill TW, Felsenberg D, Varlow J, Cooper C, Kanis JA, Silman AJ (1996) The prevalence of vertebral deformity in european men and women: the European Vertebral Osteoporosis Study. J Bone Miner Res 11(7):1010–1018

    Article  PubMed  Google Scholar 

  32. Kwok AW, Gong JS, Wang YX, et al (2012) Prevalence and risk factors of radiographic vertebral fractures in elderly Chinese men and women: results of Mr. OS (Hong Kong) and Ms. OS (Hong Kong) studies. Osteoporos Int

  33. Blank JB, Cawthon PM, Carrion-Petersen ML et al (2005) Overview of recruitment for the osteoporotic fractures in men study (MrOS). Contemp Clin Trials 26(5):557–568

    Article  PubMed  Google Scholar 

  34. Orwoll E, Blank JB, Barrett-Connor E et al (2005) Design and baseline characteristics of the osteoporotic fractures in men (MrOS) study—a large observational study of the determinants of fracture in older men. Contemp Clin Trials 26(5):569–585

    Article  PubMed  Google Scholar 

  35. Gluer CC, Eastell R, Reid DM et al (2004) Association of five quantitative ultrasound devices and bone densitometry with osteoporotic vertebral fractures in a population-based sample: the OPUS Study. J Bone Miner Res 19(5):782–793

    Article  PubMed  Google Scholar 

  36. Stewart A, Felsenberg D, Eastell R, Roux C, Gluer CC, Reid DM (2006) Relationship between risk factors and QUS in a European population: the OPUS study. Bone 39(3):609–615

    Article  CAS  PubMed  Google Scholar 

  37. Krieg MA, Comuz J, Ruffieux C, Burckhardt P (2004) Role of bone ultrasound in predicting hip fracture risk in women 70 years or older: results of the SEMOF study and comparison with literature data. Rev Med Suisse Romande 124(2):59–62

    PubMed  Google Scholar 

  38. Johansson H, Oden A, Johnell O et al (2004) Optimization of BMD measurements to identify high risk groups for treatment—a test analysis. J Bone Miner Res 19(6):906–913

    Article  PubMed  Google Scholar 

  39. McCloskey EV, Beneton M, Charlesworth D et al (2007) Clodronate reduces the incidence of fractures in community-dwelling elderly women unselected for osteoporosis: results of a double-blind, placebo-controlled randomized study. J Bone Miner Res 22(1):135–141

    Article  CAS  PubMed  Google Scholar 

  40. Kanis JA, Oden A, Johnell O, Jonsson B, de Laet C, Dawson A (2001) The burden of osteoporotic fractures: a method for setting intervention thresholds. Osteoporos Int 12(5):417–427

    Article  CAS  PubMed  Google Scholar 

  41. Breslow NE, Day NE (1987) Statistical methods in cancer research. IARC Sci Publ II(32):131–135

    Google Scholar 

  42. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560

    Article  PubMed Central  PubMed  Google Scholar 

  43. Harrell FJ (2001) General aspects of fitting regression models: regression modeling strategies. Springer Science + Business Media Inc, New York

    Book  Google Scholar 

  44. Johnell O, Kanis JA, Oden A et al (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20(7):1185–1194

    Article  PubMed  Google Scholar 

  45. Siris ES, Brenneman SK, Miller PD et al (2004) Predictive value of low BMD for 1-year fracture outcomes is similar for postmenopausal women ages 50–64 and 65 and older: results from the National Osteoporosis Risk Assessment (NORA). J Bone Miner Res 19(8):1215–1220

    Article  PubMed  Google Scholar 

  46. Stone KL, Seeley DG, Lui LY et al (2003) BMD at multiple sites and risk of fracture of multiple types: long-term results from the Study of Osteoporotic Fractures. J Bone Miner Res 18(11):1947–1954

    Article  PubMed  Google Scholar 

  47. Johnell O, Oden A, Caulin F, Kanis JA (2001) Acute and long-term increase in fracture risk after hospitalization for vertebral fracture. Osteoporos Int 12(3):207–214

    Article  CAS  PubMed  Google Scholar 

  48. Johnell O, Kanis JA, Oden A et al (2004) Fracture risk following an osteoporotic fracture. Osteoporos Int 15(3):175–179

    Article  CAS  PubMed  Google Scholar 

  49. Johansson H, Oden A, Karlsson MK, et al (2014) Waning predictive value of serum adiponectin for fracture risk in elderly men: MrOS Sweden. Osteoporos Int

  50. Johansson H, Oden A, Kanis J et al (2012) Low serum vitamin D is associated with increased mortality in elderly men: MrOS Sweden. Osteoporos Int 23(3):991–999

    Article  CAS  PubMed  Google Scholar 

  51. Luukinen H, Kakonen SM, Pettersson K et al (2000) Strong prediction of fractures among older adults by the ratio of carboxylated to total serum osteocalcin. J Bone Miner Res 15(12):2473–2478

    Article  CAS  PubMed  Google Scholar 

  52. Ivaska KK, Gerdhem P, Vaananen HK, Akesson K, Obrant KJ (2010) Bone turnover markers and prediction of fracture: a prospective follow-up study of 1040 elderly women for a mean of 9 years. J Bone Miner Res 25(2):393–403

    Article  CAS  PubMed  Google Scholar 

  53. Miller PD, Siris ES, Barrett-Connor E et al (2002) Prediction of fracture risk in postmenopausal white women with peripheral bone densitometry: evidence from the National Osteoporosis Risk Assessment. J Bone Miner Res 17(12):2222–2230

    Article  PubMed  Google Scholar 

  54. Chen JS, March LM, Cumming RG et al (2009) Role of quantitative ultrasound to predict fracture among institutionalised older people with a history of fracture. Osteoporos Int 20(1):105–112

    Article  CAS  PubMed  Google Scholar 

  55. Chen JS, Sambrook PN, Simpson JM et al (2009) Risk factors for hip fracture among institutionalised older people. Age Ageing 38(4):429–434

    Article  PubMed  Google Scholar 

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McCloskey, E.V., Kanis, J.A., Odén, A. et al. Predictive ability of heel quantitative ultrasound for incident fractures: an individual-level meta-analysis. Osteoporos Int 26, 1979–1987 (2015). https://doi.org/10.1007/s00198-015-3072-7

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