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The effect of age, weight, and lifestyle factors on calcaneal quantitative ultrasound: the ESOPO study

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Abstract

Quantitative ultrasound (QUS) techniques have been shown to be as good as bone mineral density (BMD) assessed by dual-energy X-ray absorptiometry (DXA), in predicting fracture risk: QUS technique could increase substantially the accessibility to a reliable bone osteoporosis risk evaluation, but little is know regarding the relationship of QUS to risk factors that have been found to predict DXA-BMD values and this is even more true in men. We studied 6,811 postmenopausal women 40 to 80 years of age and 4,981 men 60–80 years of age representative of the general population of all regions of Italy. All participants were questioned on lifestyle habits and on their medical history. After a physical examination "bone stiffness" (called here for simplicity, stiffness), which is derived from the values of broadband ultrasound attenuation (BUA) and speed of sounds (SoS) was measured by a heel QUS device (Achilles apparatus, Lunar, Madison, USA) . The most common recognized determinants of bone mass (either categorical or continuous variables) were modeled with stiffness by multiple regression analysis or ANOVA. Stiffness was strongly related to age and weight. After adjusting for these variables, the women who had taken hormone replacement therapy for more than a year had significantly higher stiffness values. The difference versus nonusers remained significant for up to 20 years-since-menopause (YSM). This effect was so strong that for further analysis these women were excluded. By multivariate analysis, stiffness was then found to be significantly related to recalled body weight at 25 years of age, actual and past cigarettes smoked per day, and dairy calcium intake. Stiffness was also associated with a number of categorial factors adjusted for age, weight, and YSM: prior ovariectomy, history of more than 2 months confined to bed, outdoor physical activity, smoking, chronic use of any drug, and past corticosteroid use. All these categorial and continuous variables predicted stiffness equally in men and women. In conclusion, QUS bone measurements discriminate postmenopausal women according to past use of hormone replacement therapy. Risk factors usually associated to BMD as measured by DXA are also associated to calcaneal bone stiffness as measured by QUS, and most risk factors for osteoporosis usually observed in women are equally applicable to men.

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References

  1. Hui SL, Slemenda CW, Johnston CC Jr (1988) Age and bone mass as predictors of fracture in a prospective study. J Clin Invest 81:1804–1809

    Google Scholar 

  2. Black DM, Cummings SR, Genant H, et al (1992) Axial and appendicular bone density predicts fractures in older woman. J Bone Miner Res 7:633–638

    Google Scholar 

  3. Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259

    Google Scholar 

  4. Ross PD, Davis J, Vogel J, Wasnich R (1990) A critical review of bone mass and the risk of fractures in osteoporosis. Calcif Tissue Int 46:149–161

    Google Scholar 

  5. Chandler JM, Zimmerman SI, Girman CJ, et al (2000) Low bone mineral density and risk of fracture in white female nursing home residents. JAMA 284:972–977

    Google Scholar 

  6. Paganini-Hill A, Ross PK, Gerkins VR, Henderson BE, Arthur M, Mack TM (1981) Menopausal estrogen therapy and hip fractures. Ann Intern Med 95:28–31

    Google Scholar 

  7. Cooper C, Baker DJ, Wickham C (1988) Physical activity, muscle strength, and calcium intake in fracture of the proximal femur in Britain. BMJ 1297:1443–1446

    Google Scholar 

  8. Grisso JA, Kelsey JL, Strom BL, et al (1991) Risk factors for falls as a cause of hip fracture in women. The Northeast Hip Fracture Study Group. N Engl J Med 324:1326–1331

    Google Scholar 

  9. Farmer ME, Harris T, Madans JH, Wallace RB, Cornoni-Huntley J, White LR (1989) Anthropometric indicators and hip fracture. The NHEANES I epidemiologic follow-up study. J Am Geriatr Soc 37:9–16

    Google Scholar 

  10. Kiel DP, Felson DT, Hannan MT, Anderson JJ, Wilson PW (1990) Caffeine and the risk of hip fracture: the Framingham Study. Am J Epidemiol 132:675–684

    Google Scholar 

  11. Paganini-Hill A, Chao A, Ross RK, Henderson BE (1991) Exercise and other factors in the prevention of hip fracture: the Leisure World study. Epidemiology 2:16–25

    Google Scholar 

  12. Meyer HE, Tverdal A, Falch JA (1995) Body height, body mass index, and fatal fractures: 16 years' follow-up of 674,000 Norwegian women and men. Epidemiology 6:299–305

    Google Scholar 

  13. Cummings SR, Nevitt MC, Browner WS, et al (1995) Risk factors for hip fracture in white women. N Engl J Med 332:767–73

    Google Scholar 

  14. Schott AM, Weill-Engerer S, Hans D, Duboeuf F, Delmas PD, Meunier PJ (1995) Ultrasound discriminates patients with hip fracture equally well as dual-energy X-ray absortiometry and independently of bone density. J Bone Min Res 10:243–249

    Google Scholar 

  15. Jones G, Nguyen T, Sambrook P, Kelly PJ, Eisman JA (1994) Progressive loss of bone in the femoral neck in elderly people: longitudinal findings from the Dubbo osteoporosis epidemiology study. BMJ 309:691–695

    Google Scholar 

  16. De Laet CE, Van Hout BA, Burger H, Weel AE, Hofman A, Pols HAP (1998) Hip fracture prediction in elderly men and women: validation in the Rotterdam study. J Bone Miner Res 13:1587–1593

    Google Scholar 

  17. Ross P, Huant C, Davis J, et al (1995) Predicting vertebral deformity using bone densitometry at various skeletal sites and calcaneous ultrasound. Bone 16:325–32

    Google Scholar 

  18. Melton III L, Khosla S, Atkinson E, O'Fallon W, Riggs B (1997) Relationship of bone turnover to bone density and fractures. J Bone Miner Res 12:1083–1091

    Google Scholar 

  19. Gregg EW, Kriska AM, Salomone LM, et al (1997) The epidemiology of quantitative ultrasound: a review of the relationships with bone mass, osteoporosis and fracture risk. Osteoporos Int 7:789–799

    Google Scholar 

  20. Cheng S, Tylavsky F, Carbone L (1997) Utility of ultrasound to assess risk of fracture. J Am Geriatr Soc 45:1382–1394

    Google Scholar 

  21. Frost HM (1964) Dynamics of bone remodelling. In: Frost HM (ed) Bone biodynamics. Little Brown, Boston

  22. Bauer DC, Gluer CC, Genant HK, Stone K, et al (1995) Quantitative ultrasound and vertebral fracture in postmenopausal women. J Bone Miner Res 10:353–358

    Google Scholar 

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

    Google Scholar 

  24. Turner CH, Peacock M, Timmerman L, Neal JM, Johnston CC (1995) Calcaneal ultrasonic measurements discriminate hip fracture independently of bone mass. Osteoporos Int 5:130–135

    Google Scholar 

  25. Karlsson MK, Duan Y, Ahlborg H, Obrant KJ, Johnell O, Seeman E (2001) Age, gender, and fragility fractures are associated with differences in quantitative ultrasound independent of bone mineral density. Bone 28:118–122

    Google Scholar 

  26. Mikhail MB, Flaster E, Aloia JF (1999) Stiffness in discrimination of patients with vertebral fractures. Osteoporos Int 9:24–28

    Google Scholar 

  27. Nguyen TV, Kelly PJ, Sambrook PN, Gilbert C, Pocock NA, Eisman JA (1994) Lifestyle factors and bone density in the elderly: implications for osteoporosis prevention. J Bone Miner Res 9:1339–1345

    Google Scholar 

  28. Hannan MT, Felson DT, Dawson-Hughes B, et al (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:710–720

    Google Scholar 

  29. Lunt M, Masaryk P, Scheidt-Nave C, et al (2001) The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS study. Osteoporos Int 12: 688–698

    Google Scholar 

  30. Adami S, Kanis JA. (1995) Assessment of involutional bone loss: methodological and conceptual problems. J Bone Miner Res 10:511–517

    Google Scholar 

  31. Thompson P, Taylor J, Fisher A, Oliver R (1998) Quantitative heel ultrasound in 3,180 women between 45 and 75 years of age: compliance, normal ranges and relationship to fracture history. Osteoporos Int 8: 211–214

    Google Scholar 

  32. Frost ML, Blake GM, Fogelmam I (2001) Quantitative ultrasound and bone mineral density are equally strongly associated with risk factors for osteoporosis. J Bone Miner Res 16:406–416

    Google Scholar 

  33. Ravn P, Cizza G, Bjarnason NH, et al (1999) Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women. J Bone Miner Res 14:1622–1627

    Google Scholar 

  34. Hansen M, Overgaard K, Riis B, Christiansen C (1991) Potential risk factors for development of postmenopausal osteoporosis: examined over a 12-year period. Osteoporos Int 1:95–102

    Google Scholar 

  35. Reid IR, Ames RW, Evans MC, Sharpe SJ, Gamble GD (1994) Determinants of the rate of bone loss in normal postmenopausal women. J Clin Endocrinol Metab 79:950–954

    Google Scholar 

  36. Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham Study. J Bone Miner Res 8:567–573

    Google Scholar 

  37. Nguyen TV, Center JR, Eisman JA (2000) Osteoporosis in elderly men and women: effects of dietary calcium, physical activity, and body mass index. J Bone Miner Res 15:322–331

    Google Scholar 

  38. Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138: 160–169

    Google Scholar 

  39. Blum M, Harris SS, Must A, Phillips SM, Rand WM, Dawson-Hughes B (2001) Weight and body mass index at menarche are associated with premenopausal bone mass. Osteoporos Int 12:588–594

    Google Scholar 

  40. Frost H (1993) Suggested fundamental concepts in skeletal physiology. Calcif Tissue Int 52:1–4

    Google Scholar 

  41. Lanyon LE, Rubin CT, Baust G (1986) Modulation of bone loss during calcium insufficiency by controlled dynamic loading. Calcif Tissue Int 38:209–216

    Google Scholar 

  42. Dennison E, Eastell R, Fall CHD, Kellingray S, Wood PJ, Cooper C (1999) Determinants of bone loss in elderly men and women: a prospective population-based study. Osteoporos Int 10:384–391

    Google Scholar 

  43. Nguyen TV, Sambrook PN, Eisman JA (1998) Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study. J Bone Miner Res 13:1458–1467

    Google Scholar 

  44. Blake GM, Herd RJM, Patel R, Fogelman I (2000) The effect of weight change on total body dual-energy X-ray absorptiometry: results from a clinical trial. Osteoporos Int 11:832–839

    Google Scholar 

  45. Felson DT, Zhang Y, Hannan MT, Kiel DP, Wilson PWF, Anderson JJ (1993) The effect of postmenopausal estrogen therapy on bone density in elderly women. N Engl J Med 329:1141–1146

    Google Scholar 

  46. Cauley JA, Gutai JP, Sandler RB, LaPorte RE, Kuller LH, Sashin D (1986) The relationship of endogenous estrogen to bone density and bone area in normal postmenopausal women. Am J Epidemiol 124:752–761

    Google Scholar 

  47. Kiel DP, Zhang Y, Hannan MT, Anderson JJ, Felson DT (1996) The effect of smoking at different life stages on bone mineral density in elderly men and women. Osteoporos Int 6:240–248

    Google Scholar 

  48. Burger H, de Laet C, van Daele P, et al (1998) Risk factors of increased bone loss in an elderly population: the Rotterdam Study. Am J Epidemiol 147:871–879

    Google Scholar 

  49. Hollenbach KA, Barrett-Connor E, Edelstein SL, Holbrook T (1993) Cigarette smoking and bone mineral density in older men and women. Am J Public Health 83:1265–1270

    Google Scholar 

  50. Hopper JL, Seeman E (1994) The bone density of female twins discordant for tobacco use. N Engl J Med 330:387–392

    Google Scholar 

  51. Law M, Hackshaw A (1997) A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture: recognition of a major effect. BMJ 15: 841–846

    Google Scholar 

  52. Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270

    Google Scholar 

  53. Mazess RB, Wheadon GD (1983) Immobilisation and bone. Calcif Tissue Int 35:265–267

  54. Lau E, Donnan S, Barker D, Cooper C (1988) Physical activity and calcium intake in fracture of the proximal femur in Britain. BMJ 297:1141–1143

    Google Scholar 

  55. Jaglal S, Kreiger N, Darlington C (1993) Past and recent physical activity and risk of hip fracture. Am J Epidemiol 138:107–118

    Google Scholar 

  56. Sinaki M, McPhee MC, Hodgson SF, Merritt JM, Offord KP (1986) Relationship between mineral density of spine and strength of back extensors in healthy postmenopausal women. Mayo Clin Proc 61:116–122

    Google Scholar 

  57. Yano K, Wasnich RD, Vogel JM, Heilbrun LK (1984) Bone mineral measurements among middle aged and elderly Japanese residents in Hawaii. Am J Epidemiol 119:751–763

    Google Scholar 

  58. Stillman RJ, Lohman TG, Slaughter MH, Massey BH (1986) Physical activity and bone mineral content in women aged 30 to 85 years. Med Sci Sports Exerc 18:576–580

    Google Scholar 

  59. Kanders B, Dempster DW, Lindsay R (1988) Interaction of calcium nutrition and physical activity on bone mass in young women. J Bone Miner Res 3:145–149

    Google Scholar 

  60. Pocock N, Eisman J, Gwinn T, et al (1989) Muscle strength, physical fitness and weight, but not age predict femoral neck bone mass. J Bone Miner Res 4:441–448

    Google Scholar 

  61. Sinaki M, Opitz JL, Wahner HW (1974) Bone mineral content: relationship to muscle strength in normal subjects. Arch Phys Med Rehabil 55:508–512

    Google Scholar 

  62. Kelly PJ, Pocock NA, Sambrook PN, Eisman JA (1990) Dietary calcium, sex hormones and bone mineral density in normal men. BMJ 300:1361–1364

    Google Scholar 

  63. Bauer DC, Browner WS, Cauley JA, et al (1993) Factors associated with appendicular bone mass in older women: the Study of Osteoporotic Fractures research group. Ann Intern Med 118:657–665

    Google Scholar 

  64. Cooper C, Atkinson EJ, Hensrud DD, et al (1996) Dietary protein intake and bone mass in women. Calcif Tissue Int 58:320–325

    Google Scholar 

  65. Angus RM, Sambrook PN, Pocock NA, Eisman JA (1988) Dietary calcium intake and bone mineral density. Bone Miner 4:265–277

    Google Scholar 

  66. Tylavsky FA, Anderson JJB (1988) Dietary factors in bone health of elderly lacto-ovovegetarian and omnivorous women. Am J Clin Nutr 48:842–849

    Google Scholar 

  67. Glynn NW, Meilahn EN, Charron M, Anderson SJ, Kuller LH, Cauley JA (1995) Determinants of bone mineral density in older men. J Bone Miner Res 10:1769–1777

    Google Scholar 

  68. Heaney RP, Recker RR (1986) Distribution of calcium absorption in middle-aged women. Am J Clin Nutr 43:299–305

    Google Scholar 

  69. Holbrook TL, Barrett-Connor E. A (1993) Prospective study of alcohol consumption and bone mineral density. BMJ 306:1506–1509

    Google Scholar 

  70. Hansen M, Overgaard K, Riis BJ, Christiansen C (1991) Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12-year study. BMJ 303:961–964

    Google Scholar 

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Acknowledgements

This work was totally funded by an unlimited grant from Procter & Gamble, Rome, Italy.

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Correspondence to Silvano Adami.

Appendix: Local coordinators of the ESOPO study

Appendix: Local coordinators of the ESOPO study

Antonino Accardi, Marsala; Alberto Angeli, Orbassano; Salvatore Baglio, Rome; Alfonso Baldoncini, Arezzo; Pierluigi Ballardini, Lagosanto (FE); Cataldo Bancheri, Rome; Franco Beghe, Imperia; Luigi Bernini, S. Miniato (PI); Maurizio Bevilacqua, Milan; Gerolamo Bianchi, Arenzano (GE); Giuseppe Bonomi, Palmanova (Udine); Massimo Bottai, Sarzana (SP); Giovanni Brogi, Pescia (PT); Giuseppe Candioto, Agrigento; Sergio Candiotto, Dolo (VE); Riccardo Cecchetti, Pontedera (PI); Raffaele Serqua, S.Felice a Cancello (CE); Sandro Cervelli, Rome; Stefano Coaccioli, Terni; Franco Coin, Dolo (VE); Cataldo Colella, Aversa (CE); Daniele Costi, Parma; Massimo Cravero, Torino; Salvatore D'Auria, Benevento; Giovanni D'Avola, Catania; Nicola De Gennaro, Capua (CE); Lucio Del Forno, Vasto (CH); Arturo D'Elia, Napoli; Ombretta Di Munno, Pisa; Roberto Di Virgilio, Treviso; Filippo Favazzi, Mistretta (ME); Mario Ferraris, Vercelli; Paolo Filippini, Umbertide (PG); Cristiano Maria Francucci, Ancona; Bruno Frediani, Siena; Giorgio Gandolini, Milan; Romildo Gasparini, Legnago (VR); Romeo Gatti, Viterbo; Salvatore Gatto, Napoli; Ernesto Gemini, Napoli; Tommaso Gismondi, Bari; Stefano Gonnelli, Siena; Siro Grassi, Napoli; Giovanni Iolascon, Napoli; Gian Carlo Isaia,Torino; Tommaso Izzo, Nocera Inferiore (SA); Giovanni La Montagna Renato La forgia, Matera; Giovanni Lapadula, Bari; Gaetano Loiacono Martina, Franca (TA); Pierluigi Lombardi, Castelnuovo G. (LU); Roberto Lovato, Vicenza; Riccardo Maglitto, Lentini (SR);Fabio Magnani, Vignola (MO);Nazzarena Malavolta, Bologna; Giorgio Mancini, Macerata; Giuseppe Masellis, Carpi (MO); Domenico Maugeri, Catania; Carmelo Micale, Cuggiono (MI); Redento Mora, Pavia; Maurizio Muratore, S. Cesario di Lecce (LE); Rita Occhipinti, Belluno; Geremia Oliva, Frattamaggiore (NA); Ernesto Palummeri, Genova; Domenica Panzavecchia, Partinico (PA); Salvatore Parello, Canelli (AT); Raffaele Pellerito, Torino; Giovanni Pisanu, Oristano (CA); Domenico Policicchio, Avellino; Marco Pozone, L'Aquila; Giulio Pucci, Spoleto (PG); Stefano Respizzi, Rozzano (MI); Giuseppe Roberti, Chivasso (TO); Maurizio Rossini, Verona; Sergio Rossitto, Piazza Armerina (EN); Luciano Sabadini, Arezzo; Carlo Salvarani, Reggio Emilia; Salvatore Salvini, Anzio (RM); Giuseppe SanteufemiaIglesias (CA); Ivana Santi, Milan; Leonardo Sartori, Padova; Mario Sfrappini, S. Benedetto del Tronto (AP); Ferdinando Silveri, Jesi (AN); Luigi Sinigaglia, Milano; Michele Soriano Vibo, Valentia; Ruggero Spinazzè, Conegliano (TV); Giuseppe Stancati, Cosenza; Giancarlo Tartarelli, Massa; David Topini, Viterbo; Francesco Trotta, Ferrara; Giuseppe Varcasia, Castrovillari (CS); Alfredo Zanatta, Legnago (VR).

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Adami, S., Giannini, S., Giorgino, R. et al. The effect of age, weight, and lifestyle factors on calcaneal quantitative ultrasound: the ESOPO study. Osteoporos Int 14, 198–207 (2003). https://doi.org/10.1007/s00198-002-1352-5

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