Abstract
The use of quantitative ultrasound (QUS) of the bone is rapidly gaining in popularity, and QUS is widely used worldwide for the assessment of skeletal status. Although much has been learned about the influence of various factors on ultrasonic parameters in various populations, similar information at the local level is not available. This study was carried out to examine the effects of anthropometric, dietary, physical activity, reproductive, and other lifestyle factors on QUS parameters in healthy Greek women, including children (n=217), adults (n=235), and elderly (n=369) subjects. Calcaneal QUS measurements were performed with the SAHARA device, which measures broadband ultrasound attenuation (BUA) and speed of sound (SOS) through the os calcis; a composite parameter, the quantitative ultrasound index (QUI), and an estimate of heel bone mineral density (eBMD) were also derived. All QUS indices were higher in adult women than in girls or elderly women (P<0.05). The latter had a similar BUA to girls, but lower SOS, QUI, and eBMD (P<0.05). Most QUS parameters correlated positively with height, weight, body mass index (BMI), hip circumference, organized physical activity, and activity promoting bone mass, but negatively with the time devoted to sedentary activities and absolute carbohydrate intake (P<0.05). Age of menarche and years since menopause were negatively associated with QUS in the adult and elderly women, respectively (P<0.05). The latter relationship, however, was due to the confounding effect of advancing age. Overweight and obese females had significantly higher BUA and eBMD than normal-weight subjects (P<0.05), but similar SOS and QUI; this held true for all age groups. Likewise, in all ages, individuals spending more than 2 h/week on organized activities had significantly higher QUS indices than those spending less time on exercise (P<0.05). Further, postmenarchial girls had significantly higher age-adjusted BUA, SOS, QUI, and eBMD than premenarchial ones (P<0.05). Similarly, all QUS parameters were significantly higher in adult women with an early onset of menarche (<14 years old) than in those with a late onset (P<0.05), but no effects of menarche were detected among the elderly. No significant effects of calcium intake (which was generally adequate), smoking or alcohol drinking (which were generally low) on QUS indices were observed, in either age group. Available independent variables could explain approximately 16%–24% of the total variance in BUA, SOS, QUI and eBMD. The most important positive predictors of QUS were adulthood, time devoted to organized activities, and weight or BMI, while age and carbohydrate intake per se contributed negatively. In conclusion, age, body size, physical activity, and some aspects of reproductive history and diet appear to variably affect calcaneal QUS indices among otherwise healthy Greek women at different life stages.
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References
Moyad MA (2003) Osteoporosis: a rapid review of risk factors and screening methods. Urol Oncol 21:375–379
Neville CE, Murray LJ, Boreham CA, Gallagher AM, Twisk J, Robson PJ, Savage JM, Kemper HC, Ralston SH, Davey Smith G (2002) Relationship between physical activity and bone mineral status in young adults: the Northern Ireland Young Hearts Project. Bone 30:792–798
Lazcano-Ponce E, Tamayo J, Cruz-Valdez A, Diaz R, Hernandez B, Del Cueto R, Hernandez-Avila M (2003) Peak bone mineral area density and determinants among females aged 9 to 24 years in Mexico. Osteoporos Int 14:539–547
Black DM, Arden NK, Palermo L, Pearson J, Cummings SR (1999) Prevalent vertebral deformities predict hip fractures and new vertebral deformities but not wrist fractures. Study of Osteoporotic Fractures Research Group. J Bone Miner Res 14:821–828
Uusi-Rasi K, Sievanen H, Pasanen M, Oja P, Vuori I (2002) Association of physical activity and calcium intake with the maintenance of bone mass in premenopausal women. Osteoporos Int 13:211–17
Frost ML, Blake GM, Fogelman I (2001) Quantitative ultrasound and bone mineral density are equally strongly associated with risk factors for osteoporosis. J Bone Miner Res 16:406–416
Hans D, Dargent-Molina P, Schott AM, Sebert JL, Cormier C, Kotzki PO, Delmas PD, Pouilles JM, Breart G, Meunier PJ (1996) Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study. Lancet 348:511–514
Bauer DC, Gluer CC, Cauley JA, Vogt TM, Ensrud KE, Genant HK, Black DM (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 157:629–634
Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243
Expert Panel on the Identification, Evaluation, and Treatment of Overweight in Adults (1998) Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: executive summary. Am J Clin Nutr 68:899–917
Magkos F, Manios Y, Babaroutsi E, Sidossis LS (2004) Development and validation of a food frequency questionnaire for assessing dietary calcium intake in the general population. Osteoporos Int (in press)
Groothausen J, Siemer H, Kemper HCG, Twisk J, Welten DC (1997) Influence of peak strain on lumbar bone mineral density: an analysis of 15-year physical activity in young males and females. Pediatr Exerc Sci 9:159–173
Magkos F, Manios Y, Babaroutsi E, Sidossis LS (2004) Quantitative ultrasound calcaneus measurements: normative data for the Greek population. Osteoporos Int (in press)
Yamaguchi J, Truman G, Cameron ID (2000) Lifestyle factors affecting bone ultrasonometry of the calcaneus in Japanese women. Calcif Tissue Int 66:43–46
Jakes RW, Khaw K, Day NE, Bingham S, Welch A, Oakes S, Luben R, Dalzell N, Reeve J, Wareham NJ (2001) Patterns of physical activity and ultrasound attenuation by heel bone among Norfolk cohort of European Prospective Investigation of Cancer (EPIC Norfolk): population based study. BMJ 322:140–144
Hoshino H, Kushida K, Yamazaki K, Takahashi M, Ogihara H, Naitoh K, Toyoyama O, Doi S, Tamai H, Inoue T (1996) Effect of physical activity as a caddie on ultrasound measurements of the os calcis: a cross-sectional comparison. J Bone Miner Res 11:412–418
Yanagimoto Y, Oshida Y, Sato Y (2000) Effects of walking on bone quality as determined by ultrasound in the elderly. Scand J Med Sci Sports 10:103–108
Brooke-Wavell K, Jones PR, Hardman AE, Tsuritan, Yamada Y (2001) Commencing, continuing and stopping brisk walking: effects on bone mineral density, quantitative ultrasound of bone and markers of bone metabolism in postmenopausal women. Osteoporos Int 12:581–587
Prince R, Devine A, Dick I, Criddle A, Kerr D, Kent N, Price R, Randell A (1995) The effects of calcium supplementation (milk powder or tablets) and exercise on bone density in postmenopausal women. J Bone Miner Res 10:1068–1075
Schott AM, Hans D, Sornay-Rendu E, Delmas PD, Meunier PJ (1993) Ultrasound measurements on os calcis: precision and age-related changes in a normal female population. Osteoporos Int 3:249–254
Yamazaki K, Kushida K, Ohmura A, Sano M, Inoue T (1994) Ultrasound bone densitometry of the os calcis in Japanese women. Osteoporos Int 4:220–225
Korpelainen R, Korpelainen J, Heikkinen J, Vaananen K, Keinanen-Kiukaanniemi S (2003) Lifestyle factors are associated with osteoporosis in lean women but not in normal and overweight women: a population-based cohort study of 1222 women. Osteoporos Int 14:34–43
International Obesity Task Force and European Association for the Study of Obesity (2002) Obesity in Europe—the case for action. IOTF and EASO, London (available on-line athttp://www.iotf.org/media/euobesity.pdf)
Gregg EW, Kriska AM, Salamone LM, Wolf RL, Roberts MM, Ferrell RE, Anderson SJ, Kuller LH, Cauley JA (1999) Correlates of quantitative ultrasound in the Women’s Healthy Lifestyle Project. Osteoporos Int 10:416–244
Lanyon LE (1996) Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone 18:37S–43S
Huiskes R, Ruimerman R, van Lenthe GH, Janssen JD (2000) Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405:704–706
Karlsson MK, Magnusson H, Karlsson C, Seeman E (2001) The duration of exercise as a regulator of bone mass. Bone 28:128–132
Lehtonen-Veromaa M, Mottonen T, Kautiainen H, Heinonen OJ, Viikari J (2001) Influence of physical activity and cessation of training on calcaneal quantitative ultrasound measurements in peripubertal girls: a 1-year prospective study. Calcif Tissue Int 68:146–150
Graafmans WC, Bouter LM, Lips P (1998) The influence of physical activity and fractures on ultrasound parameters in elderly people. Osteoporos Int 8:449–454
Damilakis J, Perisinakis K, Kontakis G, Vagios E, Gourtsoyiannis N (1999) Effect of lifetime occupational physical activity on indices of bone mineral status in healthy postmenopausal women. Calcif Tissue Int 64:112–116
Blanchet C, Giguere Y, Prud’homme D, Turcot-Lemay L, Dumont M, Leduc G, Cote S, Laflamme N, Rousseau F, Dodin S (2003) Leisure physical activity is associated with quantitative ultrasound measurements independently of bone mineral density in postmenopausal women. Calcif Tissue Int 73:339–349
Heinonen A, Oja P, Sievanen H, Pasanen M, Vuori I (1998) Effect of two training regimens on bone mineral density in healthy perimenopausal women: a randomized controlled trial. J Bone Miner Res 13:483–490
Paakkunainen U, Raittinen P, Viikari J, Seppanen R, Simell O (2002) The impact of low saturated fat, low cholesterol diet on bone properties measured using calcaneal ultrasound in prepubertal children. Calcif Tissue Int 71:219–226
National Institutes of Health (2000) Osteoporosis prevention, diagnosis, and therapy. NIH Consens Statement 17:1–45
Cheng S, Fan B, Wang L, Fuerst T, Lian M, Njeh C, He Y, Kern M, Lappin M, Tylavsky F, Casal D, Harris S, Genant HK (1999) Factors affecting broadband ultrasound attenuation results of the calcaneus using a gel-coupled quantitative ultrasound scanning system. Osteoporos Int 10:495–504
Adami S, Giannini S, Giorgino R, Isaia G, Maggi S, Sinigaglia L, Filipponi P, Crepaldi G, Di Munno O (2003) The effect of age, weight, and lifestyle factors on calcaneal quantitative ultrasound: the ESOPO study. Osteoporos Int 14:198–207
Krieg MA, Cornuz J, Jacquet AF, Thiebaud D, Burckhardt P (1998) Influence of anthropometric parameters and biochemical markers of bone metabolism on quantitative ultrasound of bone in the institutionalized elderly. Osteoporos Int 8:115–120
Osei-Hyiaman D, Satoshi T, Ueji M, Hideto T, Kano K (1998) Timing of menopause, reproductive years, and bone mineral density: a cross-sectional study of postmenopausal Japanese women. Am J Epidemiol 148:1055–1061
Cauley JA, Lucas FL, Kuller LH, Vogt MT, Browner WS, Cummings SR (1996) Bone mineral density and risk of breast cancer in older women: the study of osteoporotic fractures. Study of Osteoporotic Fractures Research Group. JAMA 276:1404–1408
Avioli LV (1993) Hormonal alterations and osteoporotic syndromes. J Bone Miner Res 8 [Suppl 2]:S511–514
Vogt MT, Cauley JA, Kuller LH, Nevitt MC (1997) Bone mineral density and blood flow to the lower extremities: the study of osteoporotic fractures. J Bone Miner Res 12:283–289
Cheng S, Tylavsky F, Carbone L (1997) Utility of ultrasound to assess risk of fracture. J Am Geriatr Soc 45:1382–1394
Bauer DC, Gluer CC, Genant HK, Stone K (1995) Quantitative ultrasound and vertebral fracture in postmenopausal women. Fracture Intervention Trial Research Group. J Bone Miner Res 10:353–358
Turner CH, Peacock M, Timmerman L, Neal JM, Johnson CC Jr (1995) Calcaneal ultrasonic measurements discriminate hip fracture independently of bone mass. Osteoporos Int 5:130–135
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
Mikhail MB, Flaster E, Aloia JF (1999) Stiffness in discrimination of patients with vertebral fractures. Osteoporos Int 9:24–28
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
Kiel DP, Zhang Y, Hannan MT, Anderson JJ, Baron JA, 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
Burger H, de Laet CE, van Daele PL, Weel AE, Witteman JC, Hofman A, Pols HA (1998) Risk factors for increased bone loss in an elderly population: the Rotterdam Study. Am J Epidemiol 147:871–879
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
Felson DT, Zhang Y, Hannan MT, Kannel WB, Kiel DP (1995) Alcohol intake and bone mineral density in elderly men and women. The Framingham Study. Am J Epidemiol 142:485–492
Naves Diaz M, O’Neill TW, Silman AJ (1997) The influence of alcohol consumption on the risk of vertebral deformity. European Vertebral Osteoporosis Study Group. Osteoporos Int 7:65–71
Lunt M, Masaryk P, Scheidt-Nave C, Nijs J, Poor G, Pols H, Falch JA, Hammermeister G, Reid DM, Benevolenskaya L, Weber K, Cannata J, O’Neill TW, Felsenberg D, Silman AJ, Reeve J (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
Acknowledgements
This study was supported by Friesland Hellas. The authors would like to thank Maria Bletsa, Maria Rammata, and Anastasia Doulgeri, dietitians; Silia Sidossi, research assistant; and Antigoni Tsiafitsa, technician, for their valuable help in data collection and processing.
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Babaroutsi, E., Magkos, F., Manios, Y. et al. Lifestyle factors affecting heel ultrasound in Greek females across different life stages. Osteoporos Int 16, 552–561 (2005). https://doi.org/10.1007/s00198-004-1720-4
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DOI: https://doi.org/10.1007/s00198-004-1720-4