The journal of nutrition, health & aging

, Volume 15, Issue 5, pp 404–409 | Cite as

Nutritional approach for inhibiting bone resorption in institutionalized elderly women with vitamin D insufficiency and high prevalence of fracture

  • Jean-Philippe Bonjour
  • V. Benoit
  • O. Pourchaire
  • B. Rousseau
  • J. -C. Souberbielle
Nutritional Intervention on Bone Resorption in Elderly Women



Nutritional approach to the deterioration of bone integrity and increased fracture risk appears to be particularly appropriate in elderly women living in nursing homes.


To investigate the beneficial effect of the consumption of soft plain cheese on bone resorption markers in institutionalized elderly women.


Prospective, randomized crossover controlled study.


Six French nursing homes or other institutions for elderly.


Institutionalized women ≥ 65 years old with low vitamin D status and calcium intake below 700 mg/day.


Consumption of soft plain cheese made of semi-skimmed milk which was fortified by both vitamin D3 (+ 1.25µg/100g) and milk extracted Ca, thus achieving a total Ca content of 151 mg/100g as compared to about 118 mg/100g for standard fresh cheese. Two servings were taken every day during the 6 weeks that preceded or followed a period of 6 weeks without soft plain cheese consumption.


The primary end point was the change in serum carboxy terminal cross-linked telopeptide of type I collagen (CTX) selected as a marker of bone resorption.


29 women aged 73–94 yr were selected, 21 of them with mean age 87.2±6.1 years remained compliant The intervention increased calcium and protein intakes by 51% (904±228 vs. 599±122 mg/d) and 33 % (74.2±17.1 vs. 55.6±12.7 g/d, mean±SD), respectively. The dietary intervention was associated with a statistically significant increase in serum levels of both 25OHD and IGF-I, while those of PTH, CTX and TRAP5b were significantly reduced. Compliance was 93,4 %. The daily consumption of two servings of soft plain cheese was well accepted in terms of tastiness and appetite suited portion size.


This randomized crossover controlled trial demonstrates that in elderly women living in nursing homes, the consumption of soft plain cheese increasing the supply of vitamin D, calcium and proteins, could reduce bone resorption and thereby reduce the risk of incidental fragility fractures in the long term.

Key words

Elderly women osteoporosis prevention nutritional intervention fortified cheese bone resorption 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Melton LJ, 3rd, Khosla S, Atkinson EJ, O’Fallon WM & Riggs BL (1997) Relationship of bone turnover to bone density and fractures. J Bone Miner Res 12, 1083–1091.PubMedCrossRefGoogle Scholar
  2. 2.
    Seeman E (2002) Pathogenesis of bone fragility in women and men. Lancet 359, 1841–1850.PubMedCrossRefGoogle Scholar
  3. 3.
    Delmas PD (2002) Treatment of postmenopausal osteoporosis. Lancet 359, 2018–2026.PubMedCrossRefGoogle Scholar
  4. 4.
    Seeman E & Eisman JA (2004) Treatment of osteoporosis: why, whom, when and how to treat. The single most important consideration is the individual’s absolute risk of fracture. Med J Aust 180, 298–303.PubMedGoogle Scholar
  5. 5.
    Rizzoli. R & Kraenzlin M (2007) Approaches to optimizing bone health. In The living skeleton [Roux. C, editor]. Paris, France: Wolters Kluwer Health.Google Scholar
  6. 6.
    Parikh S, Avorn J & Solomon DH (2009) Pharmacological management of osteoporosis in nursing home populations: a systematic review. J Am Geriatr Soc 57, 327–334.PubMedCrossRefGoogle Scholar
  7. 7.
    Bonjour JP, Schurch MA & Rizzoli R (1996) Nutritional aspects of hip fractures. Bone 18, 139S–144S.PubMedCrossRefGoogle Scholar
  8. 8.
    Boonen S, Bischoff-Ferrari HA, Cooper C, Lips P, Ljunggren O, Meunier PJ & Reginster JY (2006) Addressing the musculoskeletal components of fracture risk with calcium and vitamin D: a review of the evidence. Calcif Tissue Int 78, 257–270.PubMedCrossRefGoogle Scholar
  9. 9.
    Boonen S, Lips P, Bouillon R, Bischoff-Ferrari HA, Vanderschueren D & Haentjens P (2007) Need for additional calcium to reduce the risk of hip fracture with vitamin d supplementation: evidence from a comparative metaanalysis of randomized controlled trials. J Clin Endocrinol Metab 92, 1415–1423.PubMedCrossRefGoogle Scholar
  10. 10.
    Tang BM, Eslick GD, Nowson C, Smith C & Bensoussan A (2007) Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures and bone loss in people aged 50 years and older a meta-analysis. Lancet 370, 657–666.PubMedCrossRefGoogle Scholar
  11. 11.
    Dawson-Hughes B & Bischoff-Ferrari HA (2007) Therapy of osteoporosis with calcium and vitamin D. J Bone Miner Res 22Suppl 2, V59–63.PubMedCrossRefGoogle Scholar
  12. 12.
    Broe KE, Chen TC, Weinberg J, Bischoff-Ferrari HA, Holick MF & Kiel DP (2007) A higher dose of vitamin d reduces the risk of falls in nursing home residents: a randomized, multiple-dose study. J Am Geriatr Soc 55, 234–239.PubMedCrossRefGoogle Scholar
  13. 13.
    Bischoff-Ferrari HA & Staehelin HB (2008) Importance of vitamin d and calcium at older age. Int J Vitam Nutr Res 78, 286–292.PubMedCrossRefGoogle Scholar
  14. 14.
    Bonjour JP, Gueguen L, Palacios C, Shearer MJ & Weaver CM (2009) Minerals and vitamins in bone health: the potential value of dietary enhancement. Br J Nutr 101, 1581–1596.PubMedCrossRefGoogle Scholar
  15. 15.
    Bonjour JP, Schurch MA, Chevalley T, Ammann P & Rizzoli R (1997) Protein intake, IGF-1 and osteoporosis. Osteoporoslnt? Suppl 3, S36–42.Google Scholar
  16. 16.
    Heaney RP (2001) Protein intake and bone health: the influence of belief systems on the conduct of nutritional science. Am J Clin Nutr 73, 5–6.PubMedGoogle Scholar
  17. 17.
    Bell J & Whiting SJ (2002) Elderly women need dietary protein to maintain bone mass. Nutr Rev 60, 337–341.PubMedCrossRefGoogle Scholar
  18. 18.
    Bonjour JP (2005) Dietary protein: an essential nutrient for bone health. J Am Coll Nutr 24, 526S–536S.PubMedGoogle Scholar
  19. 19.
    Heaney RP & Layman DK (2008) Amount and type of protein influences bone health. Am J Clin Nutr 87, 1567S–1570S.PubMedGoogle Scholar
  20. 20.
    Morgan KT (2008) Nutritional determinants of bone health. J Nutr Elder 27, 3–27.PubMedCrossRefGoogle Scholar
  21. 21.
    Gaffney-Stomberg E, Insogna KL, Rodriguez NR & Keistetter JE (2009) Increasing dietary protein requirements in elderly people for optimal muscle and bone health. J Am Geriatr Soc 57, 1073–1079.PubMedCrossRefGoogle Scholar
  22. 22.
    Palacios S, Castelo-Branco C, Cifuentes I, von Heide S, Baro L, Tapia-Ruano C, Menendez C & Rueda C (2005) Changes in bone turnover markers after calcium-enriched milk supplementation in healthy postmenopausal women: a randomized, double-blind prospective clinical trial. Menopause 12, 63–68.PubMedCrossRefGoogle Scholar
  23. 23.
    Bonjour JP, Brandolini-Bunlon M, Boirie Y, Morel-Laporte F, Braesco V, Bertiere MC & Souberbielle JC (2008) Inhibition of bone turnover by milk intake in postmenopausal women Br J Nutr 100, 866–874.PubMedCrossRefGoogle Scholar
  24. 24.
    Heaney RP, McCarron DA, Dawson-Hughes B, Oparil S, Berga SL, Stem JS, Barr SI & Rosen CJ (1999) Dietary changes favorably affect bone remodeling in older adults. J Am Diet Assoc 99, 1228–1233.PubMedCrossRefGoogle Scholar
  25. 25.
    Bonjour JP, Benoit V, Pourchare O, Ferry M, Rousseau B & Souberbielle JC (2009) Inhibition of markers of bone resorption by consumption of vitamin D and calcium-fortified soft plain cheese by institutionalised elderly women. Br J Nutr 102, 962–966PubMedCrossRefGoogle Scholar
  26. 26.
    Henriksen K, Tanko LB, Qvist P, Delmas PD, Christiansen C & Karsdal MA (2007) Assessment of osteoclast number and function: application in the development of new and improved treatment modalities for bone diseases. Osteoporos Int 18, 681–685.PubMedCrossRefGoogle Scholar
  27. 27.
    Fardellone P, Sebert JL, Bouraya M, Bonidan O, Leclercq G, Doutrellot C, Bellony R & Dubreuil A (1991) Evaluation of the calcium content of diet by frequential self-questionnaire. Rev Rhum Mai Osteoartic58, 99–103.Google Scholar
  28. 28.
    Guigoz Y, Lauque S & Vellas BJ (2002) Identifying the elderly at risk for malnutritioa The Mini Nutritional Assessment. Clin Geriatr Med 18, 737–757.PubMedCrossRefGoogle Scholar
  29. 29.
    Gascoin-Lachambre G, Trivin C, Brauner R & Souberbielle JC (2007) Serum procollagen type 1 amino-terminal propeptide (P1NP) as an early predictor of the growth response to growth hormone treatment: Comparison of intrauterine growth retardation and idiopathic short stature. Growth Horm IGF Res 7, 194–200.CrossRefGoogle Scholar
  30. 30.
    Hollis BW, Kamerad JQ, Selvaag SR Lorenz JD & Napoli JL (1993) Determination of vitamin D status by radioimmunoassay with an 125I-labeled tracer. Clin Chem 39, 529–533.PubMedGoogle Scholar
  31. 31.
    Zochling J, Chen JS, Seibel M, Schwarz J, Cameron ED, Gumming RG, March L & Sambrook PN (2005) Calcium metabolism in the frail elderly. Clin Rheumatol 24, 576–582.PubMedCrossRefGoogle Scholar
  32. 32.
    Pauly L, Stehle P & Volkert D (2007) Nutritional situation of elderly nursing home residents. Z Gerontol Geriatr 40, 3–12.PubMedCrossRefGoogle Scholar
  33. 33.
    Abellan van Kan G, Gambassi G, de Groot LC et al. (2008) Nutrition and aging. The Carla Workshop. J Nutr Health Aging 12, 355–364.PubMedCrossRefGoogle Scholar
  34. 34.
    Lengyel CO, Whiting SJ & Zello GA (2008) Nutrient inadequacies among elderly residents of long-term care facilities. Can J Diet Pract Res 69, 82–88.PubMedCrossRefGoogle Scholar
  35. 35.
    Bruyere O, Decock C, Delhez M, Collette J & Reginster JY (2009) Highest prevalence of vitamin D inadequacy in institutionalized women compared with noninstitutionalized women: a case-control study. Womens Health (Lond Engl) 5, 49–54.Google Scholar
  36. 36.
    Rapp K, Becker C, Lamb SE, Icks A & Klenk J (2008) Hip fractures in institutionalized elderly people: incidence rates and excess mortality. J Bone Miner Res 23, 1825–1831.PubMedCrossRefGoogle Scholar
  37. 37.
    Guilley E, Chevalley T, Herrmann F, Baccino D, Hoffmeyer P, Rapin CH & Rizzoli R (2008) Reversal of the hip fracture secular trend is related to a decrease in the incidence in institution-dwelling elderly women. Osteoporos Int 19, 1741–1747.PubMedCrossRefGoogle Scholar
  38. 38.
    Nakamura K, Oyama M, Takahashi S, Yoshizawa Y, Kobayashi R Oshiki R, Saito T & Tsuchiya Y (2009) Fracture incidence in nursing homes in Japan. Osteoporos Int.Google Scholar
  39. 39.
    Kanis JA, McCloskey EV, Johansson H, Strom O, Borgstrom F & Oden A (2008) Case finding for the management of osteoporosis with FRAX—assessment and intervention thresholds for the UK. Osteoporos Int 19, 1395–1408.PubMedCrossRefGoogle Scholar
  40. 40.
    Gamero P, Hausherr E, Chapuy MC et al. (1996) Markers of bone resorption predict hip fracture in elderly women: the EPIDOS Prospective Study. J Bone Miner Res 11, 1531–1538.Google Scholar
  41. 41.
    Garnero P, Sornay-Rendu E, Duboeuf F & Delmas PD (1999) Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study. J Bone Miner Res 14, 1614–1621.PubMedCrossRefGoogle Scholar
  42. 42.
    Chapurlat RD, Gamero P, Breart G, Meunier PJ & Delmas PD (2000) Serum type I collagen breakdown product (serum CTX) predicts hip fracture risk in elderly women: the EPIDOS study. Bone 27, 283–286.PubMedCrossRefGoogle Scholar
  43. 43.
    Bruyere O, Collette J, Delmas P, Rouillon A, Roux C, Seidel L, Richy F & Reginster JY (2003) Interest of biochemical markers of bone turnover for long-term prediction of new vertebral fracture in postmenopausal osteoporotic women. Maturitas 44, 259–265.PubMedCrossRefGoogle Scholar
  44. 44.
    Ravn P, Thompson DE, Ross PD & Christiaasen C (2003) Biochemical markers for prediction of 4-year response in bone mass during bisphosphonate treatment for prevention of postmenopausal osteoporosis. Bone 33, 150–158.PubMedCrossRefGoogle Scholar
  45. 45.
    Hannon RA & Eastell R (2003) Biochemical markers of bone turnover and fracture prediction. J Br Menopause Soc 9, 10–15.PubMedCrossRefGoogle Scholar
  46. 46.
    Bauer DC, Black DM, Garnero P, Hochberg M, Ott S, Orloff J, Thompson DE, Ewing SK & Delmas PD (2004) Change in bone turnover and hip, non-spine, and vertebral fracture in alendronate-treated women: the fracture intervention trial. J Bone Miner Res 19, 1250–1258.PubMedCrossRefGoogle Scholar
  47. 47.
    Greenspan SL, Resnick NM & Parker RA (2005) Early changes in biochemical markers of bone turnover are associated with long-term changes in bone mineral density in elderly women on alendronate, hormone replacement therapy, or combination therapy: a three-year, double-blind, placebo-controlled, randomized clinical trial. J Clin Endocrinol Metab 90, 2762–2767.PubMedCrossRefGoogle Scholar
  48. 48.
    Cremers S & Garnero P (2006) Biochemical markers of bone turnover in the clinical development of drugs for osteoporosis and metastatic bone disease: potential uses and pitfalls. Drags 66, 2031–2058.CrossRefGoogle Scholar
  49. 49.
    Wang J, Lee J, Burns D, Doherty D, Brunner L, Peterson M & DeSilva B (2009) “Fit-for-purpose” method validation and application of a biomarker (C-terminal telopeptides of type 1 collagen) in denosumab clinical studies. Aaps J 11, 385–394.PubMedCrossRefGoogle Scholar
  50. 50.
    Delmas PD, Bjamason NH, Mitlak BH, Ravoux AC, Shah AS, Huster WJ, Draper M & Christiansen C (1997) Effects of raloxifene on bone mineral density, serum cholesterol concentrations, and uterine endometrium in postmenopausal women. N Engl J Med 337, 1641–1647.PubMedCrossRefGoogle Scholar
  51. 51.
    Lindsay R Gallagher JC, Kleerekoper M & Pickar JH (2002) Effect of lower doses of conjugated equine estrogens with and without medroxyprogesterone acetate on bone in early postmenopausal women. Jama 287, 2668–2676.PubMedCrossRefGoogle Scholar
  52. 52.
    Meunier PJ, Roux C, Seeman E et al. (2004) The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. N Engl J Med 350, 459–468.PubMedCrossRefGoogle Scholar
  53. 53.
    Grados F, Brazier M, Kamel S, Mathieu M, Hurtebize N, Maamer M, Garabedian M, Sebert JL & Fardellone P (2003) Prediction of bone mass density variation by bone remodeling markers in postmenopausal women with vitamin D insufficiency treated with calcium and vitamin D supplementation. J Clin Endocrinol Metab 88, 5175–5179.PubMedCrossRefGoogle Scholar
  54. 54.
    Asp NG & Contor L (2003) Process for Assessment of Scientific Support for Claims on Food (PASSCLAIM): overall introduction. Eur J Nutr 42Suppl 1, I3–I5.PubMedGoogle Scholar
  55. 55.
    Prentice A, Bonjour JP, Branca F, Cooper C, Flynn A, Garabedian M, Muller D, Pannemans D & Weber P (2003) PASSCLAIM — Bone health and osteoporosis. Eur J Nutr 42Suppl 1, I28–I49.PubMedGoogle Scholar
  56. 56.
    Chevalley T, Hoffmeyer P, Bonjour JP & Rizzoli R (2010) Early serum IGF-I response to oral protein supplements in elderly women with a recent hip fracture. Clin Nutr 29, 78–83.PubMedCrossRefGoogle Scholar
  57. 57.
    Chevalley T, Rizzoli R, Manen D, Caverzasio J & Bonjour JP (1998) Arginine increases insulin-like growth factor-I production and collagen synthesis in osteoblast-like cells. Bone 23, 103–109.PubMedCrossRefGoogle Scholar
  58. 58.
    Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford AP, Casperson SL, Jiang J, Chinkes DL & Urban RJ (2009) Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in olderwomen. J Clin Endocrinol Metab 94, 1630–1637.PubMedCrossRefGoogle Scholar
  59. 59.
    Martin AD (2001) Apports nutritionnels conseillés pour la population française, 3ème édition éd: TEC&DOC, Paris.Google Scholar

Copyright information

© Serdi and Springer Verlag France 2011

Authors and Affiliations

  • Jean-Philippe Bonjour
    • 2
    • 1
    • 6
  • V. Benoit
    • 3
    • 1
  • O. Pourchaire
    • 4
    • 1
  • B. Rousseau
    • 3
    • 1
  • J. -C. Souberbielle
    • 5
    • 1
  1. 1.University Hospitals and Faculty of MedicineGenevaSwitzerland
  2. 2.Division of Bone DiseasesWHO Collaborating Center for Osteoporosis PreventionGenevaSwitzerland
  3. 3.Groupe de Recherche Nutritionnelle, YoplaitBoulogneFrance
  4. 4.Hôpital Local Intercommunal de MorestelMorestelFrance
  5. 5.Laboratoire d’Explorations FonctionnellesHôpital Necker-Enfant MaladesParisFrance
  6. 6.Division of Bone DiseasesGeneva University Hospitals and Faculty of MedicineGeneva 14Switzerland

Personalised recommendations