Skip to main content

Advertisement

SpringerLink
Log in

Fermented dairy products consumption is associated with attenuated cortical bone loss independently of total calcium, protein, and energy intakes in healthy postmenopausal women

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

A longitudinal analysis of bone microstructure in postmenopausal women of the Geneva Retirees Cohort indicates that age-related cortical bone loss is attenuated at non-bearing bone sites in fermented dairy products consumers, not in milk or ripened cheese consumers, independently of total energy, calcium, or protein intakes.

Introduction

Fermented dairy products (FDP), including yogurts, provide calcium, phosphorus, and proteins together with prebiotics and probiotics, all being potentially beneficial for bone. In this prospective cohort study, we investigated whether FDP, milk, or ripened cheese consumptions influence age-related changes of bone mineral density (BMD) and microstructure.

Methods

Dietary intakes were assessed at baseline and after 3.0 ± 0.5 years with a food frequency questionnaire in 482 postmenopausal women enrolled in the Geneva Retirees Cohort. Cortical (Ct) and trabecular (Tb) volumetric (v) BMD and microstructure at the distal radius and tibia were assessed by high-resolution peripheral quantitative computerized tomography, in addition to areal (a) BMD and body composition by dual-energy X-ray absorptiometry, at the same time points.

Results

At baseline, FDP consumers had lower abdominal fat mass and larger bone size at the radius and tibia. Parathyroid hormone and β-carboxyterminal cross-linked telopeptide of type I collagen levels were inversely correlated with FDP consumption. In the longitudinal analysis, FDP consumption (mean of the two assessments) was associated with attenuated loss of radius total vBMD and of Ct vBMD, area, and thickness. There was no difference in aBMD and at the tibia. These associations were independent of total energy, calcium, or protein intakes. For other dairy products categories, only milk consumption was associated with lower decrease of aBMD and of failure load at the radius.

Conclusion

In this prospective cohort of healthy postmenopausal women, age-related Ct bone loss was attenuated at non-bearing bone sites in FDP consumers, not in milk or ripened cheese consumers, independently of total energy, calcium, or protein intakes.

Study registration

ISRCTN11865958 (http://www.isrctn.com)

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Rizzoli R (2014) Dairy products, yogurts, and bone health. Am J Clin Nutr 99(5 Suppl):1256s–1262s. https://doi.org/10.3945/ajcn.113.073056

    Article  PubMed  CAS  Google Scholar 

  2. Rizzoli R, Biver E (2017) Effects of fermented milk products on bone. Calcif Tissue Int 102:489–500. https://doi.org/10.1007/s00223-017-0317-9

    Article  PubMed  CAS  Google Scholar 

  3. Sahni S, Mangano KM, Tucker KL, Kiel DP, Casey VA, Hannan MT (2014) Protective association of milk intake on the risk of hip fracture: results from the Framingham Original Cohort. J Bone Miner Res 29(8):1756–1762. https://doi.org/10.1002/jbmr.2219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Sahni S, Mangano KM, Kiel DP, Tucker KL, Hannan MT (2017) Dairy intake is protective against bone loss in older vitamin D supplement users: the Framingham study. J Nutr 147(4):645–652. https://doi.org/10.3945/jn.116.240390

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Laird E, Molloy AM, McNulty H, Ward M, McCarroll K, Hoey L, Hughes CF, Cunningham C, Strain JJ, Casey MC (2017) Greater yogurt consumption is associated with increased bone mineral density and physical function in older adults. Osteoporos Int 28(8):2409–2419. https://doi.org/10.1007/s00198-017-4049-5

    Article  PubMed  CAS  Google Scholar 

  6. Bischoff-Ferrari HA, Dawson-Hughes B, Baron JA, Kanis JA, Orav EJ, Staehelin HB, Kiel DP, Burckhardt P, Henschkowski J, Spiegelman D, Li R, Wong JB, Feskanich D, Willett WC (2011) Milk intake and risk of hip fracture in men and women: a meta-analysis of prospective cohort studies. J Bone Miner Res 26(4):833–839. https://doi.org/10.1002/jbmr.279

    Article  PubMed  CAS  Google Scholar 

  7. Michaëlsson K, Wolk A, Langenskiöld S, Basu S, Warensjö Lemming E, Melhus H, Byberg L (2014) Milk intake and risk of mortality and fractures in women and men: cohort studies. BMJ 349:g6015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Fung TT, Meyer HE, Willett WC, Feskanich D (2017) Protein intake and risk of hip fractures in postmenopausal women and men age 50 and older. Osteoporos Int 28(4):1401–1411. https://doi.org/10.1007/s00198-016-3898-7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Sahni S, Tucker KL, Kiel DP, Quach L, Casey VA, Hannan MT (2013) Milk and yogurt consumption are linked with higher bone mineral density but not with hip fracture: the Framingham Offspring Study. Arch Osteoporos 8(1–2):119. https://doi.org/10.1007/s11657-013-0119-2

    Article  PubMed  PubMed Central  Google Scholar 

  10. Byberg L, Bellavia A, Larsson SC, Orsini N, Wolk A, Michaelsson K (2016) Mediterranean diet and hip fracture in Swedish men and women. J Bone Miner Res 31(12):2098–2105. https://doi.org/10.1002/jbmr.2896

    Article  PubMed  CAS  Google Scholar 

  11. Durosier-Izart C, Biver E, Merminod F, van Rietbergen B, Chevalley T, Herrmann FR, Ferrari SL, Rizzoli R (2017) Peripheral skeleton bone strength is positively correlated with total and dairy protein intakes in healthy postmenopausal women. Am J Clin Nutr 105(2):513–525. https://doi.org/10.3945/ajcn.116.134676

    Article  PubMed  CAS  Google Scholar 

  12. Morin P, Herrmann F, Ammann P, Uebelhart B, Rizzoli R (2005) A rapid self-administered food frequency questionnaire for the evaluation of dietary protein intake. Clin Nutr 24(5):768–774. https://doi.org/10.1016/j.clnu.2005.03.002

    Article  PubMed  Google Scholar 

  13. Hercberg S, Preziosi P, Briancon S, Galan P, Triol I, Malvy D, Roussel AM, Favier A (1998) A primary prevention trial using nutritional doses of antioxidant vitamins and minerals in cardiovascular diseases and cancers in a general population: the SU.VI.MAX study—design, methods, and participant characteristics. SUpplementation en VItamines et Mineraux AntioXydants. Control Clin Trials 19(4):336–351

    Article  PubMed  CAS  Google Scholar 

  14. Durosier C, van Lierop A, Ferrari S, Chevalley T, Papapoulos S, Rizzoli R (2013) Association of circulating sclerostin with bone mineral mass, microstructure, and turnover biochemical markers in healthy elderly men and women. J Clin Endocrinol Metab 98(9):3873–3883

    Article  PubMed  CAS  Google Scholar 

  15. Chevalley T, Bonjour JP, van Rietbergen B, Ferrari S, Rizzoli R (2013) Fracture history of healthy premenopausal women is associated with a reduction of cortical microstructural components at the distal radius. Bone 55(2):377–383. https://doi.org/10.1016/j.bone.2013.04.025

    Article  PubMed  CAS  Google Scholar 

  16. Biver E, Durosier C, Chevalley T, Herrmann FR, Ferrari S, Rizzoli R (2015) Prior ankle fractures in postmenopausal women are associated with low areal bone mineral density and bone microstructure alterations. Osteoporos Int 26(8):2147–2155. https://doi.org/10.1007/s00198-015-3119-9

    Article  PubMed  CAS  Google Scholar 

  17. Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK (2010) Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone 47(3):519–528. https://doi.org/10.1016/j.bone.2010.05.034

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ellouz R, Chapurlat R, van Rietbergen B, Christen P, Pialat JB, Boutroy S (2014) Challenges in longitudinal measurements with HR-pQCT: evaluation of a 3D registration method to improve bone microarchitecture and strength measurement reproducibility. Bone 63:147–157. https://doi.org/10.1016/j.bone.2014.03.001

    Article  PubMed  Google Scholar 

  19. Vico L, Zouch M, Amirouche A, Frere D, Laroche N, Koller B, Laib A, Thomas T, Alexandre C (2008) High-resolution pQCT analysis at the distal radius and tibia discriminates patients with recent wrist and femoral neck fractures. J Bone Miner Res 23(11):1741–1750. https://doi.org/10.1359/jbmr.080704

    Article  PubMed  Google Scholar 

  20. Ainsworth BE, Haskell WL, Leon AS, Jacobs DR Jr, Montoye HJ, Sallis JF, Paffenbarger RS Jr (1993) Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 25(1):71–80

    Article  PubMed  CAS  Google Scholar 

  21. Lippuner K, Johansson H, Kanis JA, Rizzoli R (2010) FRAX assessment of osteoporotic fracture probability in Switzerland. Osteoporos Int 21(3):381–389

    Article  PubMed  CAS  Google Scholar 

  22. Shah RV, Murthy VL, Allison MA, Ding J, Budoff M, Frazier-Wood AC, Lima JA, Steffen L, Siscovick D, Tucker KL, Ouyang P, Abbasi SA, Danielson K, Jerosch-Herold M, Mozaffarian D (2016) Diet and adipose tissue distributions: the multi-ethnic study of atherosclerosis. Nutr Metab Cardiovasc Dis 26(3):185–193. https://doi.org/10.1016/j.numecd.2015.12.012

    Article  PubMed  CAS  Google Scholar 

  23. Karpe F, Pinnick KE (2015) Biology of upper-body and lower-body adipose tissue—link to whole-body phenotypes. Nat Rev Endocrinol 11(2):90–100. https://doi.org/10.1038/nrendo.2014.185

    Article  PubMed  CAS  Google Scholar 

  24. Gijsbers L, Ding EL, Malik VS, de Goede J, Geleijnse JM, Soedamah-Muthu SS (2016) Consumption of dairy foods and diabetes incidence: a dose-response meta-analysis of observational studies. Am J Clin Nutr 103(4):1111–1124. https://doi.org/10.3945/ajcn.115.123216

    Article  PubMed  CAS  Google Scholar 

  25. Sluijs I, Forouhi NG, Beulens JW, van der Schouw YT, Agnoli C, Arriola L, Balkau B, Barricarte A, Boeing H, Bueno-de-Mesquita HB, Clavel-Chapelon F, Crowe FL, de Lauzon-Guillain B, Drogan D, Franks PW, Gavrila D, Gonzalez C, Halkjaer J, Kaaks R, Moskal A, Nilsson P, Overvad K, Palli D, Panico S, Quiros JR, Ricceri F, Rinaldi S, Rolandsson O, Sacerdote C, Sanchez MJ, Slimani N, Spijkerman AM, Teucher B, Tjonneland A, Tormo MJ, Tumino R, van der AD, Sharp SJ, Langenberg C, Feskens EJ, Riboli E, Wareham NJ (2012) The amount and type of dairy product intake and incident type 2 diabetes: results from the EPIC-InterAct Study. Am J Clin Nutr 96(2):382–390. https://doi.org/10.3945/ajcn.111.021907

    Article  PubMed  CAS  Google Scholar 

  26. Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, Muller R, Zhao B, Guo X, Lang T, Saeed I, Liu XS, Guo XE, Cremers S, Rosen CJ, Stein EM, Nickolas TL, McMahon DJ, Young P, Shane E (2013) Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab 98(6):2562–2572. https://doi.org/10.1210/jc.2013-1047

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Liu CT, Broe KE, Zhou Y, Boyd SK, Cupples LA, Hannan MT, Lim E, McLean RR, Samelson EJ, Bouxsein ML, Kiel DP (2017) Visceral adipose tissue is associated with bone microarchitecture in the Framingham Osteoporosis Study. J Bone Miner Res 32(1):143–150. https://doi.org/10.1002/jbmr.2931

    Article  PubMed  CAS  Google Scholar 

  28. Machado LG, Domiciano DS, Figueiredo CP, Caparbo VF, Takayama L, Oliveira RM, Lopes JB, Menezes PR, Pereira RM (2016) Visceral fat measured by DXA is associated with increased risk of non-spine fractures in nonobese elderly women: a population-based prospective cohort analysis from the Sao Paulo Ageing & Health (SPAH) Study. Osteoporos Int 27(12):3525–3533. https://doi.org/10.1007/s00198-016-3682-8

    Article  PubMed  CAS  Google Scholar 

  29. Vitezova A, Muka T, Zillikens MC, Voortman T, Uitterlinden AG, Hofman A, Rivadeneira F, Kiefte-de Jong JC, Franco OH (2017) Vitamin D and body composition in the elderly. Clin Nutr 36(2):585–592. https://doi.org/10.1016/j.clnu.2016.04.017

    Article  PubMed  CAS  Google Scholar 

  30. Burton KJ, Rosikiewicz M, Pimentel G, Butikofer U, von Ah U, Voirol MJ, Croxatto A, Aeby S, Drai J, McTernan PG, Greub G, Pralong FP, Vergeres G, Vionnet N (2017) Probiotic yogurt and acidified milk similarly reduce postprandial inflammation and both alter the gut microbiota of healthy, young men. Br J Nutr 117(9):1312–1322. https://doi.org/10.1017/s0007114517000885

    Article  PubMed  CAS  Google Scholar 

  31. Lisko DJ, Johnston GP, Johnston CG (2017) Effects of dietary yogurt on the healthy human gastrointestinal (GI) microbiome. Microorganisms 5(1):E6. https://doi.org/10.3390/microorganisms5010006

    Article  PubMed  CAS  Google Scholar 

  32. Panahi S, Fernandez MA, Marette A, Tremblay A (2017) Yogurt, diet quality and lifestyle factors. Eur J Nutr 71(5):573–579. https://doi.org/10.1038/ejcn.2016.214

    Article  CAS  Google Scholar 

  33. Wang H, Livingston KA, Fox CS, Meigs JB, Jacques PF (2013) Yogurt consumption is associated with better diet quality and metabolic profile in American men and women. Nutr Res 33(1):18–26. https://doi.org/10.1016/j.nutres.2012.11.009

    Article  PubMed  CAS  Google Scholar 

  34. Cormier H, Thifault E, Garneau V, Tremblay A, Drapeau V, Perusse L, Vohl MC (2016) Association between yogurt consumption, dietary patterns, and cardio-metabolic risk factors. Eur J Nutr 55(2):577–587. https://doi.org/10.1007/s00394-015-0878-1

    Article  PubMed  CAS  Google Scholar 

  35. Tremblay A, Panahi S (2017) Yogurt consumption as a signature of a healthy diet and lifestyle. J Nutr 147(7):1476s–1480s. https://doi.org/10.3945/jn.116.245522

    Article  PubMed  CAS  Google Scholar 

  36. Langsetmo L, Barr SI, Berger C, Kreiger N, Rahme E, Adachi JD, Papaioannou A, Kaiser SM, Prior JC, Hanley DA, Kovacs CS, Josse RG, Goltzman D (2015) Associations of protein intake and protein source with bone mineral density and fracture risk: a population-based cohort study. J Nutr Health Aging 19(8):861–868. https://doi.org/10.1007/s12603-015-0544-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E (2010) Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet 375(9727):1729–1736. https://doi.org/10.1016/s0140-6736(10)60320-0

    Article  PubMed  Google Scholar 

  38. Nilsson M, Sundh D, Mellstrom D, Lorentzon M (2017) Current physical activity is independently associated with cortical bone size and bone strength in elderly Swedish women. J Bone Miner Res 32(3):473–485. https://doi.org/10.1002/jbmr.3006

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are indebted to M.-A. Schaad, RN, and A. Sigaud, RN, for the management of participants, to C. Genet, G. Conicella, and J. Lang for DXA and HR-pQCT measurements and to Dr. P. Lescuyer, PhD, for the serum determinations. We thank the Swiss Foundation for Research on Ageing AETAS for the kind supply of its mobile osteodensitometer. We also thank Roche-Diagnostic, which provided some assay reagents.

Funding

This study received support from the Geneva University Hospitals and Faculty of Medicine Clinical Research Center, Danone and the Yogurt in Nutrition Initiative, and the BNP-Paribas Foundation. None of the funders had any influence on the study design, implementation, and analysis, and on interpretation of the data.

Author information

Authors and Affiliations

  1. Division of Bone Diseases, Department of Internal Medicine Specialties, Geneva University Hospitals and Faculty of Medicine, University of Geneva, 4 Rue Gabrielle Perret-Gentil, 1205, Geneva, Switzerland

    E. Biver, C. Durosier-Izart, F. Merminod, T. Chevalley, S.L. Ferrari & R. Rizzoli

  2. Department of Biomedical Engineering, Eindhoven University of Technology, 5600 MB, Eindhoven, The Netherlands

    B. van Rietbergen

Authors
  1. E. Biver
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Durosier-Izart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Merminod
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Chevalley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. van Rietbergen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S.L. Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Rizzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Biver.

Ethics declarations

All subjects signed a written informed consent before undergoing a series of interviews and assessments. The study protocol has received the approval from the Geneva University Hospitals’ Ethics Committee.

Conflicts of interest

Emmanuel Biver received a grant from the Yogurt in Nutrition Initiative for this research project. René Rizzoli received fees from Danone, Nestlé, and CNIEL for lectures or advisory boards, outside the submitted work. Bert van Rietbergen is a consultant for Scanco Medical AG, outside the submitted work; Claire Durosier-Izart, Fanny Merminod, Thierry Chevalley, and Serge Ferrari declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(DOCX 32.1 kb)

ESM 2

(DOCX 29.1 kb)

ESM 3

(DOCX 28.8 kb)

ESM 4

(DOCX 33.6 kb)

ESM 5

(DOCX 22.9 kb)

ESM 6

(DOCX 24.6 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Biver, E., Durosier-Izart, C., Merminod, F. et al. Fermented dairy products consumption is associated with attenuated cortical bone loss independently of total calcium, protein, and energy intakes in healthy postmenopausal women. Osteoporos Int 29, 1771–1782 (2018). https://doi.org/10.1007/s00198-018-4535-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-018-4535-4

Keywords

Search

Navigation