Osteoporosis International

, Volume 16, Issue 9, pp 1016–1023 | Cite as

Two-year changes in bone and body composition in young children with a history of prolonged milk avoidance

  • J. E. P. Rockell
  • S. M. Williams
  • R. W. Taylor
  • A. M. Grant
  • I. E. Jones
  • A. Goulding
Original Article

Abstract

No previous longitudinal studies of calcium intake, anthropometry and bone health in young children with a history of avoiding cow’s milk have been undertaken. We report the 2-year changes of a group of 46 Caucasian children (28 girls, l8 boys) aged 8.1±2.0 years (mean ± SD) who had low calcium intakes at baseline and were short in stature, with elevated body mass index, poor skeletons and lower Z scores for both areal bone mineral density (BMD, in grams per square centimeter) and volumetric density (bone mineral apparent density, BMAD, in grams per cubic centimeter), compared with a reference population of milk drinkers. At follow-up, adverse symptoms to milk had diminished and modest increases in milk consumption and calcium intake had occurred. Total body bone mineral content (BMC) and bone area assessed by dual energy X-ray absorptiometry had increased (P<0.05), and calcium intake from all sources was associated with both these measures (P<0.05). However, although some catch-up in height had taken place, the group remained significantly shorter than the reference population (Z scores −0.39±1.14), with elevated body mass index (Z scores 0.46±1.0). The ultradistal radius BMC Z scores remained low (−0.31±0.98). The Z scores for BMD had improved to lie within the normal range at predominantly cortical sites (33% radius, neck of femur and hip trochanter) but had worsened at predominantly trabecular sites (ultradistal radius and lumbar spine), where values lay below those of the reference group (P<0.05). Similarly, although volumetric BMAD Z scores at the 33% radius had normalized, BMAD Z scores at the lumbar spine remained below the reference population at follow-up (−0.67±1.12, P<0.001). Our results demonstrate persisting height reduction, overweight and osteopenia at the ultradistal radius and lumbar spine in young milk avoiders over 2 years of follow-up.

Keywords

Bone density change Calcium Children Height Milk Protein 

References

  1. 1.
    Eastell R, Lambert H (2002) Diet and healthy bones. Calcif Tissue Int 70:400–404CrossRefPubMedGoogle Scholar
  2. 2.
    Goulding A, Rockell JEP, Black RE, Grant AM, Jones IE, Williams SM (2004) Children who avoid drinking cow’s milk are at increased risk for prepubertal bone fractures. J Am Diet Assoc 104:250–253CrossRefPubMedGoogle Scholar
  3. 3.
    Chan GM, Hoffman K, McMurry M (1994) Effects of dairy products on bone and body composition in pubertal girls. J Pediatr 126:551–556Google Scholar
  4. 4.
    Cadogan J, Eastell R, Jones N, Barker ME (1997) Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. BMJ 315:1255–1260PubMedGoogle Scholar
  5. 5.
    Merrilees MJ, Smart EJ, Gilchrist NL, Frampton C, Turner JG, Hooke E, March RL, Maguire P (2000) Effects of dairy food supplements on bone mineral density in teenage girls. Eur J Nutr 39:256–262CrossRefPubMedGoogle Scholar
  6. 6.
    Du XQ, Greenfield H, Fraser DR, Ge KY, Liu ZH, He W (2002) Milk consumption and bone mineral content in Chinese adolescent girls. Bone 30:521–528CrossRefPubMedGoogle Scholar
  7. 7.
    Bonjour J-P, Chevalley T, Ammann P, Slosman D, Rizzoli R (2001) Gain in bone mineral mass in prepubertal girls 3.5 years after discontinuation of calcium supplementation: a follow-up study. Lancet 358:1208–1212CrossRefPubMedGoogle Scholar
  8. 8.
    Sandler RB, Slemenda CW, LaPorte RE, Cauley JA, Schramm MM, Baresi ML, Kriska AM (1985) Postmenopausal bone density and milk consumption in childhood and adolescence. Am J Clin Nutr 42:270–274PubMedGoogle Scholar
  9. 9.
    Murphy S, Khaw K-T, May H, Compston JE (1994) Milk consumption and bone mineral density in middle aged and elderly women. BMJ 308:939–941PubMedGoogle Scholar
  10. 10.
    Soroko S, Horbrook TL, Edelstein S, Barrett-Connor E (1994) Lifetime milk consumption and bone mineral density in older women. Am J Public Health 84:1319–1322PubMedGoogle Scholar
  11. 11.
    Nieves J, Gildon A, Siris E, Kelsey J, Lindsay R (1995) Teenage and current calcium intakes are related to bone mineral density in college females. Med Sci Sports Exerc 27:178–182Google Scholar
  12. 12.
    Teegarden D, Lyle RM, Proulx WR, Johnston CC, Weaver CM (1999) Previous milk consumption is associated with greater bone density in young women. Am J Clin Nutr 69:1014–1017PubMedGoogle Scholar
  13. 13.
    Matkovic V, Landoll JD, Badenhop-Stevens NE, Ha E-Y, Crncevic-Orlic Z, Li B, Goel P (2004) Nutrition influences skeletal development from childhood to adulthood: a study of hip, spine, and forearm in adolescent females. J Nutr 134:701S–705SPubMedGoogle Scholar
  14. 14.
    Kalkwarf HJ, Khoury JC, Lanphear BP (2003) Milk intake during childhood and adolescence, adult bone density, and osteoporotic fractures in US women. Am J Clin Nutr 77:257–265PubMedGoogle Scholar
  15. 15.
    Weinsier RL, Krumdieck CL (2000) Dairy foods and bone health: examination of the evidence. Am J Clin Nutr 72:681–689PubMedGoogle Scholar
  16. 16.
    Feskanich D, Willett WC, Colditz GA (2003) Calcium, vitamin D, milk consumption, and hip fractures: a prospective study among postmenopausal women. Am J Clin Nutr 77:504–511PubMedGoogle Scholar
  17. 17.
    Ministry of Health (2003) NZ food NZ children: key results of the 2002 National Children’s Nutrition Survey. In: Ministry of Health, Wellington, pp 1–267Google Scholar
  18. 18.
    Henderson RC, Hayes PR (1994) Bone mineralization in children and adolescents with a milk allergy. Bone Miner 27:1–12PubMedGoogle Scholar
  19. 19.
    Stallings VA, Oddleifson NW, Negrini BY, Zemel BS, Wellens R (1994) Bone mineral content and dietary calcium intake in children prescribed a low-lactose diet. J Pediatr Gastroenterol Nutr 18:440–445PubMedGoogle Scholar
  20. 20.
    Infante D, Tormo R (2000) Risk of inadequate bone mineralization in diseases involving long-term suppression of dairy products. J Pediatr Gastroenterol Nutr 30:310–313CrossRefPubMedGoogle Scholar
  21. 21.
    Black RE, Williams SM, Jones IE, Goulding A (2002) Children who avoid drinking cow milk have low dietary calcium intakes and poor bone health. Am J Clin Nutr 76:675–680PubMedGoogle Scholar
  22. 22.
    Hidvegi E, Arato A, Cserhati E, Horvath C, Szabo A, Szabo A (2003) Slight decrease in bone mineralization in cow milk-sensitive children. J Pediatr Gastroenterol Nutr 36:44–49CrossRefPubMedGoogle Scholar
  23. 23.
    Host A (1994) Cow’s milk protein allergy and intolerance in infancy. Some clinical, epidemiological and immunological aspects. Pediatr Allergy Immunol 5:5S–36SGoogle Scholar
  24. 24.
    Taylor R, Goulding A (1998) Validation of a short food frequency questionnaire to assess calcium intake in children aged 3 to 6 years. Eur J Clin Nutr 52:464–465CrossRefPubMedGoogle Scholar
  25. 25.
    Tanner JM (1962) Growth at adolescence. Blackwell Scientific Publications, OxfordGoogle Scholar
  26. 26.
    Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920PubMedGoogle Scholar
  27. 27.
    Goulding A, Jones IE, Taylor RW, Manning PJ, Williams SM (2001) Bone mineral density and body composition in boys with distal forearm fractures: a dual-energy X-ray absorptiometry study. J Pediatr 139:509–515CrossRefPubMedGoogle Scholar
  28. 28.
    Goulding A, Cannan R, Williams SM, Gold EJ, Taylor RW, Lewis-Barned NJ (1998) Bone mineral density in girls with forearm fractures. J Bone Miner Res 13:143–148PubMedGoogle Scholar
  29. 29.
    Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243CrossRefPubMedGoogle Scholar
  30. 30.
    Khosla S, Melton LJ, Dekutoski MB, Achenbach SJ, Oberg AL, Riggs BL (2003) Incidence of childhood distal forearm fractures over 30 years. A population-based study. JAMA 290:1479–1485CrossRefPubMedGoogle Scholar
  31. 31.
    Goldberg JP, Folta SC, Must A (2002) Milk: can a “good” food be so bad? Pediatrics 110:826–831CrossRefPubMedGoogle Scholar
  32. 32.
    Whiting SJ, Vatanparast H, Baxter-Jones A, Faulkner RA, Mirwald R, Bailey DA (2004) Factors that affect bone mineral accrual in the adolescent growth spurt. J Nutr 134:696S–700SPubMedGoogle Scholar
  33. 33.
    Host A, Halken S, Jacobsen HP, Christensen AE, Herskind AM, Plesner K (2002) Clinical course of cow’s milk protein allergy/intolerance and atopic diseases in childhood. Pediatr Allergy Immunol 13:23–28CrossRefPubMedGoogle Scholar
  34. 34.
    Birch LL, Fisher JO (1998) Development of eating behaviors among children and adolescents. Pediatrics 101:539–549PubMedGoogle Scholar
  35. 35.
    Fisher JO, Mitchell DC, Smiciklas-Wright H, Mannino ML, Birch LL (2004) Meeting calcium recommendations during middle childhood reflects mother–daughter beverage choices and predicts bone mineral status. Am J Clin Nutr 79:698–706PubMedGoogle Scholar
  36. 36.
    Heaney R (1994) The bone-remodeling transient: implications for the interpretation of clinical studies of bone mass change. J Bone Miner Res 9:1515–1523PubMedGoogle Scholar
  37. 37.
    Docio S, Riancho JA, Perez A, Olmos JM, Amado JA, Gonzalez-Macias J (1998) Seasonal deficiency of vitamin D in children: a potential target for osteoporosis-preventing strategies? J Bone Miner Res 13:544–548PubMedGoogle Scholar
  38. 38.
    Zamora SA, Rizzoli R, Belli DC, Slosman DO, Bonjour J-P (1999) Vitamin D supplementation during infancy is associated with higher bone mineral mass in prepubertal girls. J Clin Endocrinol 84:4541–4544CrossRefPubMedGoogle Scholar
  39. 39.
    Di Stefano M, Veneto G, Malservisi S, Cecchetti L, Minguzzi L, Strocchi A, Corazza GR (2002) Lactose malabsorption and intolerance and peak bone mass. Gastroenterology 122:1793–1799PubMedGoogle Scholar
  40. 40.
    Parfitt AM (1994) The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4:382–398PubMedGoogle Scholar
  41. 41.
    Goulding A (2003) Milk components and bone health. Aust J Dairy Technol 58:73–78Google Scholar
  42. 42.
    Naylor KE, Rogers A, Fraser RB, Hall V, Eastell R, Blumsohn A (2003) Serum osteoprotegerin as a determinant of bone metabolism in a longitudinal study of human pregnancy and lactation. J Clin Endocrinol Metab 88:5361–5365CrossRefPubMedGoogle Scholar
  43. 43.
    Cornish J, Callon K, Banovic T, Bava U, Watson M, Chen Q, Palmano K, Haggarty W, Grey AB, Reid IR (2002) Lactoferrin is a potent osteoblast/chondrocyte growth factor, inhibits osteoclastogenesis and is anabolic to bone in vivo. J Bone Miner Res 17:SU151Google Scholar
  44. 44.
    Yamamura J, Aoe S, Toba Y, Motouri M, Kawakami H, Kumegawa M, Itabashi A, Takada Y (2002) Milk basic protein (MBP) increases radial bone mineral density in healthy adult women. Biosci Biotechnol Biochem 66:702–704CrossRefPubMedGoogle Scholar
  45. 45.
    Banu J, Wang L, Kalu DN (2003) Effects of increased muscle mass on bone in male mice overexpressing IGF-I in skeletal muscles. Calcif Tissue Int 73:196–201CrossRefPubMedGoogle Scholar
  46. 46.
    Libanati C, Baylink DJ, Lois-Wenzel E, Srinivasan N, Mohan S (1999) Studies on the potential mediators of skeletal changes occurring during puberty in girls. J Clin Endocrinol Metab 84:2807–2814CrossRefPubMedGoogle Scholar
  47. 47.
    Kasukawa Y, Baylink DJ, Wergedal JE, Amaar Y, Srivastava AK, Guo RQ, Mohan S (2003) Lack of insulin-like growth factor 1 exaggerates the effect of calcium deficiency on bone accretion in mice. Endocrinology 144:4682–4689CrossRefPubMedGoogle Scholar
  48. 48.
    Leighton G, Clark ML (1929) Milk consumption and the growth of school-children; second preliminary report on tests to Scottish Board of Health. Lancet i:40–43CrossRefGoogle Scholar
  49. 49.
    Paganus A, Juntunen-Backman K, Savilahti E (1992) Follow-up of nutritional status and dietary survey in children with cow’s milk allergy. Acta Paediatr 81:518–521PubMedGoogle Scholar
  50. 50.
    Tiainen JM, Nuutinen OM, Kalavainen MP (1995) Diet and nutritional status in children with cow’s milk allergy. Eur J Clin Nutr 49:605–612PubMedGoogle Scholar
  51. 51.
    Isolauri E, Satas Y, Salo MK, Isosomppi R, M K (1998) Elimination diet in cow’s milk allergy: risk for impaired growth in young children. J Pediatr 132:1004–1009PubMedGoogle Scholar
  52. 52.
    Parsons T, Van Dusseldorp M, Van der Vliet M, Van de Werken K, Schaafsma G, Van Staveren W (1997) Reduced bone mass in Dutch adolescents fed a macrobiotic diet in early life. J Bone Miner Res 12:1486–1494PubMedGoogle Scholar
  53. 53.
    Zemel MB, Shi H, Greer B, Dirienzo D, Zemel PC (2000) Regulation of adiposity by dietary calcium. FASEB J 14:1132–1138Google Scholar
  54. 54.
    Parikh SJ, Yanovski JA (2003) Calcium intake and adiposity. Am J Clin Nutr 77:281–287PubMedGoogle Scholar
  55. 55.
    Fuchs RK, Bauer JJ, Snow CM (2001) Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res 16:148–156PubMedGoogle Scholar
  56. 56.
    Petit MA, McKay HA, MacKelvie KJ, Heinonen A, Khan KM, Beck TJ (2002) A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. J Bone Miner Res 17:363–372PubMedGoogle Scholar
  57. 57.
    Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E (1999) The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest 104:795–804PubMedGoogle Scholar
  58. 58.
    Adams P, Berridge FR (1969) Effects of kwashiorkor on cortical and trabecular bone. Arch Dis Child 44:705–709PubMedGoogle Scholar
  59. 59.
    Lee WT, Leung SS, Lui SS, Lau J (1993) Relationship between long-term calcium intake and bone mineral content of children aged from birth to 5 years. Br J Nutr 70:235–248PubMedGoogle Scholar
  60. 60.
    Rauch F, Neu C, Manz F, Shoenau E (2001) The development of metaphyseal cortex—implications for distal radius fractures during growth. J Bone Miner Res 16:1547–1555PubMedGoogle Scholar
  61. 61.
    Currey JD (2003) How well are bones designed to resist fracture? J Bone Miner Res 18:591–598PubMedGoogle Scholar
  62. 62.
    Goulding A, Jones IE, Taylor RW, Manning PJ, Williams SM (2000) More broken bones: a 4-year double cohort study of young girls with and without distal forearm fractures. J Bone Miner Res 15:2011–2018PubMedGoogle Scholar
  63. 63.
    Davidson PL, Goulding A, Chalmers DJ (2003) Biomechanical analysis of arm fracture in obese boys. J Paediatr Child Health 39:657–664CrossRefPubMedGoogle Scholar
  64. 64.
    Jones IE, Williams SM, Goulding A (2004) Associations of birth weight and length, childhood size and smoking with bone fractures during growth: evidence from a birth cohort study. Am J Epidemiol 159:343–350CrossRefPubMedGoogle Scholar
  65. 65.
    Karlsson M, Weigall SJ, Duan Y, Seeman E (2000) Bone size and volumetric density in women with anorexia nervosa receiving estrogen replacement therapy and in women recovered from anorexia nervosa. J Clin Endocrinol Metab 85:3177–3182CrossRefPubMedGoogle Scholar
  66. 66.
    Heaney RP (2002) Ethnicity, bone status, and the calcium requirement. Nutr Res 22:153–178CrossRefGoogle Scholar
  67. 67.
    Opotowsky AR, Bilezikian JP (2003) Racial differences in the effect of early milk consumption on peak and postmenopausal bone mineral density. J Bone Miner Res 18:1978–1988PubMedGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2004

Authors and Affiliations

  • J. E. P. Rockell
    • 1
  • S. M. Williams
    • 2
  • R. W. Taylor
    • 1
  • A. M. Grant
    • 3
  • I. E. Jones
    • 3
  • A. Goulding
    • 3
  1. 1.Department of Human NutritionUniversity of OtagoDunedinNew Zealand
  2. 2.Department of Preventive and Social MedicineUniversity of OtagoDunedinNew Zealand
  3. 3.Department of Medical and Surgical SciencesUniversity of OtagoDunedinNew Zealand

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