Research Article| Volume 56, ISSUE 6, P591-597, June 2003

Ultrasound bone measurement in children and adolescents

Correlation with nutrition, puberty, anthropometry, and physical activity


      Ultrasound bone measurement in healthy Croatian children and adolescents has been evaluated. Relationships between pubertal status, anthropometry, nutrition, and physical activity with ultrasound bone parameter were analyzed. A total number of 501 children and adolescents of both sexes participated in the study. There were 244 prepubertal children (120 boys and 122 girls) and 259 postpubertal adolescents (112 boys and 147 girls). Anthropometric measurements included height, weight, percent of fat tissue, and body mass index. Quantitative ultrasound measurements of the heel (nondominant side) were performed using “Sahara” sonometer and included speed of sound (SOS), broad-band ultrasound attenuation (BUA), and calculated bone stiffness (QUI). Dietary data were assessed using specially designed semiquantitative food frequency questionnaire calculations based on the daily intakes of calcium, carbohydrates, fats, and proteins. Quantitative ultrasound bone measurements (BUA, SOS, and QUI) were similar in prepubertal boys and girls. Adolescent boys had significantly higher BUA (P<.01) than girls. The percentage of children and adolescents who consumed more than 1,000 mg of calcium per day were 54.8% and 48.7%, respectively. Body weight and pubertal status and activity were significantly correlated with bone stiffness but not the calcium intake. In this study, bone stiffness in children and adolescents is determined by pubertal status and body weight, rather than by calcium intake.


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        • Ruiz J.C
        • Mandel C
        • Garabedian M
        Influence of spontaneous calcium intake and physical exercise on the vertebral and femoral bone mineral density of children and adolescents.
        J Bone Miner Res. 1995; 10: 675-682
        • Katzman D.K
        • Bachrach L.K
        • Carter D.R
        • Marcus R
        Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls.
        J Clin Endocrinol Metab. 1991; 73: 1332-1339
        • Glastre K
        • Braillon P
        • David L
        • Cochat P
        • Meunier P.J
        • Delmas P.D
        Measurement of bone mineral content of the lumbar spine by dual energy x-ray absorptiometry in normal children: correlations with growth parameters.
        J Clin Endocrinol Metab. 1990; 70: 1330-1333
        • Lonzer D
        • Imrie R
        • Rogers D
        • Worley D
        • Licata A
        • Secic M
        Effects of heredity, age, weight, puberty, activity and calcium intake on bone mineral density in children.
        Clin Pediatr (Phila). 1996; 35: 185-189
        • Lloyd T
        • Andon M.B
        • Rollings N
        • Martel J.K
        • Landis R.J
        • Demers L.M
        • Eggli D.F
        • Kieselhorst K
        • Kulin H.E
        Calcium supplementation and bone mineral density in adolescent girls.
        JAMA. 1993; 270: 841-844
        • Chan G
        Dietary calcium and bone mineral status of children and adolescents.
        Am J Dis Child. 1991; 145: 631-634
        • Cadogan J.R
        • Eastell N
        • Jones M.E
        • Barker
        Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial.
        BMJ. 1997; 315: 1255-1260
        • Gunnes M
        • Lehmann E.H
        Physical activity and dietary constituents as predictors of forearm cortical and trabecular bone gain in healthy children and adolescents: a prospective study.
        Acta Pediatr Jpn. 1996; 85: 19-25
        • Goulding A
        • Cannan R
        • Williams S.M
        • Gold E.J
        • Taylor R.W
        • Lewis-Barned N.J
        Bone mineral density in girls with forearm fractures.
        J Bone Miner Res. 1998; 13: 143-148
        • Caulfield L.E
        • Himes J.H
        • Rivera J.A
        Nutritional supplementation during early childhood and bone mineralization during adolescence.
        J Nutr. 1995; 125: 1104S
        • Heaney R.P
        Nutrition and risk for osteoporosis.
        Academic Press, San Diego1996
        • Chan G.M
        • Hess M
        • Hollis J
        • Book L.S
        Bone mineral status in childhood accidental fractures.
        Am J Dis Child. 1984; 138: 569-570
        • Bonjour J.P
        • Theintz G
        • Buchs B
        • Slosman D
        • Rizzoli R
        Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence.
        J Clin Endocrinol Metab. 1991; 73: 555-563
        • Theintz G
        • Buchs B
        • Rizzoli R
        • Slosman D
        • Clavien H
        • Sizonenko P.C
        • Bonjour J.P
        Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects.
        J Clin Endocrinol Metab. 1992; 75: 1060-1065
        • Takahashi Y
        • Minamitani K
        • Kobayashi Y
        • Minagawa M
        • Yasuda T
        • Niimi H
        Spinal and femoral bone mass accumulation during normal adolescence—comparison with female patients with sexual precocity and with hypogonadism.
        J Clin Endocrinol Metab. 1996; 81: 1248-1253
        • Baroncelli G.I
        • Saggese G
        Critical ages and stages of puberty in the accumulation of spinal and femoral bone mass: the validity of bone mass measurements.
        Horm Res. 2000; 54: 2-8
        • Riggs L.B
        • Melton J.L
        Osteoporosis. Etiology, diagnosis and management.
        Lippincot-Raven, Philadelphia1995
        • Kaufman J.J
        • Einhorn T.A
        Ultrasound assessment of bone.
        J Bone Miner Res. 1993; 8: 517-525
        • Duquette J
        • Lin J
        • Hoffman A
        • Houde J
        • Ahmadi S
        • Baran D
        Correlations among bone mineral density, broadband ultrasound attenuation, mechanical indentation testing, and bone orientation in bovine femoral neck samples.
        Calcif Tissue Int. 1997; 60: 181-186
        • Gluer C.C
        • Wu C.Y
        • Genant H.K
        Broadband ultrasound attenuation signals depend on trabecular orientation: an in vitro study.
        Osteoporos Int. 1993; 3: 185-188
        • Baran D.T
        • McCarthy C.K
        • Leahey D
        • Lew R
        Broadband ultrasound attenuation of the calcaneus predicts lumbar and femoral neck density in Caucasian women: a preliminary study.
        Osteoporos Int. 1991; 1: 110-113
        • Lochmuller E.M
        • Zeller J.B
        • Kaiser D
        • Eckstein F
        • Landgraf J
        • Putz R
        • Steldinger R
        Correlation of femoral and lumbar DXA and calcaneal ultrasound, measured in situ with intact soft tissues, with the in vitro failure loads of the proximal femur.
        Osteoporos Int. 1998; 8: 591-598
        • Jaworski M
        • Lebiedowski M
        • Lorenc R.S
        • Trempe J
        Ultrasound bone measurements in pediatric subjects.
        Calcif Tissue Int. 1995; 56: 368-371
        • Mughal M.Z
        • Langton C.M
        • Utretch G
        • Morrison J
        • Specker B.L
        Comparison between broad-band ultrasound attenuation of the calcaneum and total body bone mineral density in children.
        Acta Pediatr Jpn. 1996; 85: 663-665
        • Marshall W.A
        • Tanner J.M
        Variations in the pattern of pubertal changes in girls.
        Arch Dis Child. 1970; 45: 291-294
        • Marshall W.A
        • Tanner J.M
        Variations in the pattern of pubertal changes in boys.
        Arch Dis Child. 1970; 45: 13-15
        • Pennington J.A.T
        Methods for obtaining food consumption information.
        Springer-Verlag, Berlin1991
        • Kulier I
        Nutritive tables (Prehrambene tablice).
        Diana, Zagreb1990
      1. U.S.D.A. Nutritive value of food. Home and Garden Bulletin. 1977; No.72.

        • Colić I
        Nutritional value of meals in social nourishment for students and establishing the normative. Master's Thesis.
        University of Zagreb, 1987
        • The National Academy of Science
        Recommended dietary allowance.
        National Academy Press, Washington, DC1989
        • The Ministry of Health
        Regulation of the health accuracy of food (Pravilnik o zdravstvenoj ispravnosti dijetetskih namirnica).
        Narodne novine, Zagreb1994 (No. 46)
        • Yates A.A
        • Schilcker S.A
        • Suitor C.W
        Dietary reference intakes: the new basis for recommendations for calcium and related nutrients, B vitamins, and choline.
        J Am Diet Assoc. 1998; 98: 699-706
        • Kang C
        • Paley M
        • Ordrige R
        • Speller R
        In vivo MRI measurements of bone quality in the calcaneus: a comparison with DXA and ultrasound.
        Osteoporos Int. 1999; 9: 65-74
        • Trebacz H
        • Natali A
        Ultrasound velocity and attenuation in cancellous bone samples from lumbar vertebra and calcaneus.
        Osteoporos Int. 1999; 9: 99-103
        • Lochmuller E.-M
        • Eckstein F
        • Zeller J.-B
        • Steldinger R
        • Putz R
        Comparison of quantitative ultrasound in the human calcaneus with mechanical failure loads of the hip and spine.
        Ultrasound Obstet Gynaecol. 1999; 14: 125-133
        • Boot A
        • Ridder M.A.J
        • Pols H.A.P
        • Krenning E.P
        • Muinck S
        • Keizer
        Bone mineral density in children and adolescents: relation to puberty, calcium intake and physical activity.
        J Clin Endocrinol Metab. 1997; 82: 57-62
        • Wang M.C
        • Moore E.C
        • Craword P.B
        • Hudes M
        • Sabry Z.I
        • Marcus R
        • Bachrach L.K
        Influence of pre-adolescent diet on quantitative ultrasound measurements of the calcaneus in young adult women.
        Osteoporos Int. 1999; 9: 532-535
        • Paakkunainen U
        • Raittinen P
        • Viikari J
        • Seppanen R
        • Simell O
        The impact of low-saturated fat, low-cholesterol diet on bone properties measured using calcaneal ultrasound in pre-pubertal children.
        Calcif Tissue Int. 2002; 71: 219-226
        • Lehtonen-Veromaa M
        • Mottonen T
        • Kautianen H
        • Heinonen O.J
        • Viikari J
        Influence of physical activity on ultrasound and dual-energy x-ray absorptiometry bone measurements in peripubertal girls: a cross sectional study.
        Calcif Tissue Int. 2000; 66: 248-254
        • Daly R.M
        • Rich P.A
        • Klein R
        Influence of high impact loading on ultrasound bone measurements in children: a cross-sectional report.
        Calcif Tissue Int. 1997; 60: 401-404
        • Baroncelli G.I
        • Federico G
        • Bertelloni S
        • de Terlizzi F
        • Cadossi R
        • Saggese S
        Bone quality assessment by quantitative ultrasound of proximal phalanxes of the hand in healthy subjects aged 3–21 years.
        Pediatr Res. 2001; 49: 713-718
        • Kovačić L
        Production and consumption of milk in Croatia.
        Mljekarstvo. 1995; 42: 269-279
        • European Communities
        Healthy food for Europe's citizens.
        Publication Unit, Brussels2000
        • Nicklas T.A
        Dietary studies of children—the Bogalusa Heart Study experience.
        J Am Diet Assoc. 1995; 95: 1127-1133
        • Crawley H.F
        • Summerbaell D
        The nutrient and food intakes of British male dieters aged 16–17 years.
        J Hum Nutr Diet. 1998; 11: 33-40
        • Whitney E.N
        • Rolfes S.R
        Understanding nutrition.
        3rd ed. An International Thomas Publishing Co, Belmont1999
        • Zemel M.B
        Calcium utilization: effect of varying level and source of dietary protein.
        Am J Clin Nutr. 1988; 48: 880-883
        • Abelow B.J
        • Holford T.R
        • Insogna K.L
        Cross-cultural association between dietary animal protein and hip fracture: a hypothesis.
        Calcif Tissue Int. 1992; 50: 14-18
        • Feskanich D
        • Rimm E.B
        • Giovannucci E.L
        • Colditz G.A
        • Stampfer M.J
        • Litin L.B
        • Willett W.C
        Reproducibility and validity of food intake measurements from a semiquantitative food frequency questionnaire.
        J Am Diet Assoc. 1993; 93: 790-796
        • Green T.J
        • Allen O.B
        • O'Connor D.L
        A three-day weighed food record and a semiquantitative food-frequency questionnaire are valid measures for assessing the folate and vitamin B-12 intakes of women aged 16 to 19 years.
        J Nutr. 1998; 128: 1665-1671
        • McCann S.E
        • Trevisan M
        • Priore R.L
        • Muti P
        • Marković N
        • Russell M
        • Chan A.W.K
        • Freudenheim J.L
        Comparability of nutrient estimation by three food frequency questionnaires for use in epidemiological studies.
        Nutr Cancer Int J. 1999; 34: 4-9
        • Serra Majem L.S
        • Morales D
        • Domingo C
        • Caubet E
        • Ribas L
        • Nouges R.M
        Comparison of 2 methods of evaluation of food and nutrient intake: 24-hour recall and semiquantitative frequency questionnaire.
        Med Clin (Barc). 1995; 104: 16
        • Schaefer E.J
        • Augustin J.L
        • Schaefer M.M
        • Rasmussen H
        • Ordovas J.M
        • Dallal G.E
        • Dwyer J.T
        Lack of efficacy of a food-frequency questionnaire in assessing dietary macronutrient intakes in subjects consuming diets of known composition.
        Am J Clin Nutr. 2000; 71: 746-751
        • Friis S
        • Kjaer S.K
        • Stripp C
        Reproducibility and relative validity of a self-administered semiquantitative food frequency questionnaire applied to younger women.
        J Clin Epidemiol. 1997; 50: 303-311
        • Gnardellis C
        • Trichopoulou A
        • Katsouyanni K
        • Polychronopoulos E
        • Rimm E.B
        • Trichopoulos D
        Reproducibility and validity of an extensive semiquantitative food frequency questionnaire among Greek school teachers.
        Epidemiology. 1995; 6: 74-77
        • Taylor R.W
        • Goulding A
        Validation of a short food frequency questionnaire to assess calcium intake in children aged 3 to 6 years.
        Eur J Clin Nutr. 1998; 52: 464
        • Balli F
        • Viola L
        • Di Biase A.R
        • Tarozzi G
        Nutritional status and dietary habits of children in the Province of Modena.
        Pediatr Med Chir. 1999; 21: 13-15
        • Doyle E.I
        • Feldman R.H.L
        Factors affecting nutrition behavior among middle-class adolescents in urban area of Northern region of Brazil.
        Rev Saude Publica. 1997; 31: 342-347
        • Johnston C.C
        • Miller J.Z
        • Slemenda C.W
        • Reister T.K
        • Hui S
        • Christian J.C
        • Peackock M
        Calcium supplementation and increases in bone mineral density in children.
        N Engl J Med. 1992; 327: 82-87
        • Lloyd T
        • Martel J.K
        • Rollings N
        • Andon M.B
        • Kulin H
        • Demers L.M
        • Eggli D.F
        • Kieselhorst K
        • Chinchilli V.M
        The effect of calcium supplementation and Tanner stage on bone density, content and area in teenage women.
        Osteoporos Int. 1996; 6: 276-283