Skip to main content

Advertisement

SpringerLink
Log in

Effects of Fermented Milk Products on Bone

  • Review
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Fermented milk products like yogurt or soft cheese provide calcium, phosphorus, and protein. All these nutrients influence bone growth and bone loss. In addition, fermented milk products may contain prebiotics like inulin which may be added to yogurt, and provide probiotics which are capable of modifying intestinal calcium absorption and/or bone metabolism. On the other hand, yogurt consumption may ensure a more regular ingestion of milk products and higher compliance, because of various flavors and sweetness. Bone mass accrual, bone homeostasis, and attenuation of sex hormone deficiency-induced bone loss seem to benefit from calcium, protein, pre-, or probiotics ingestion, which may modify gut microbiota composition and metabolism. Fermented milk products might also represent a marker of lifestyle promoting healthy bone health.

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

Similar content being viewed by others

References

  1. Salque M, Bogucki PI, Pyzel J, Sobkowiak-Tabaka I, Grygiel R, Szmyt M, Evershed RP (2013) Earliest evidence for cheese making in the sixth millennium BC in northern Europe. Nature 493(7433):522–525. doi:10.1038/nature11698

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46(2):294–305. doi:10.1016/j.bone.2009.10.005

    Article  PubMed  Google Scholar 

  4. Weaver CM (2015) Diet, gut microbiome, and bone health. Curr Osteoporos Rep 13(2):125–130. doi:10.1007/s11914-015-0257-0

    Article  PubMed  PubMed Central  Google Scholar 

  5. 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(11):1978–1988. doi:10.1359/jbmr.2003.18.11.1978

    Article  PubMed  Google Scholar 

  6. Goulding A, Rockell JE, 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(2):250–253. doi:10.1016/j.jada.2003.11.008

    Article  PubMed  Google Scholar 

  7. Handel MN, Heitmann BL, Abrahamsen B (2015) Nutrient and food intakes in early life and risk of childhood fractures: a systematic review and meta-analysis. Am J Clin Nutr 102(5):1182–1195. doi:10.3945/ajcn.115.108456

    Article  CAS  PubMed  Google Scholar 

  8. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R (2008) High-protein intake enhances the positive impact of physical activity on BMC in prepubertal boys. J Bone Miner Res 23(1):131–142. doi:10.1359/jbmr.070907

    Article  CAS  PubMed  Google Scholar 

  9. Chevalley T, Bonjour JP, van Rietbergen B, Ferrari S, Rizzoli R (2014) Tracking of environmental determinants of bone structure and strength development in healthy boys: an eight-year follow up study on the positive interaction between physical activity and protein intake from prepuberty to mid-late adolescence. J Bone Miner Res 29(10):2182–2192. doi:10.1002/jbmr.2247

    Article  CAS  PubMed  Google Scholar 

  10. Chevalley T, Bonjour JP, Audet MC, Merminod F, van Rietbergen B, Rizzoli R, Ferrari S (2017) Prepubertal impact of protein intake and physical activity on weight-bearing peak bone mass and strength in males. J Clin Endocrinol Metab 102(1):157–166. doi:10.1210/jc.2016-2449

    PubMed  Google Scholar 

  11. Matkovic V, Landoll JD, Badenhop-Stevens NE, Ha EY, 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(3):701s–705s

    Article  PubMed  Google Scholar 

  12. Wiley AS (2005) Does milk make children grow? Relationships between milk consumption and height in NHANES 1999-2002. Am J Hum Biol 17(4):425–441. doi:10.1002/ajhb.20411

    Article  PubMed  Google Scholar 

  13. Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27(4):1281–1386. doi:10.1007/s00198-015-3440-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 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. doi:10.1007/s12603-015-0544-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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. doi:10.3945/ajcn.116.134676

    Article  CAS  PubMed  Google Scholar 

  16. Radavelli-Bagatini S, Zhu K, Lewis JR, Prince RL (2014) Dairy food intake, peripheral bone structure, and muscle mass in elderly ambulatory women. J Bone Miner Res 29(7):1691–1700. doi:10.1002/jbmr.2181

    Article  CAS  PubMed  Google Scholar 

  17. 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. doi:10.3945/jn.116.240390

    Article  CAS  PubMed  Google Scholar 

  18. 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. doi:10.1007/s00198-017-4049-5

    Article  CAS  PubMed  Google Scholar 

  19. Biver E, Durosier-Izart C, Merminod F, Chevalley T, Ferrari S, Rizzoli R (2017) Fermented dairy products consumption is associated with attenuated cortical bone loss independently of total calcium, protein and energy intakes in postmenopausal women. World Congress on Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (WCO-IOF-ESCEO 2017): Oral Communication Abstracts. Osteoporos Int. doi: 10.1007/s00198-017-3945-z

  20. 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(1):78–83. doi:10.1016/j.clnu.2009.07.003

    Article  CAS  PubMed  Google Scholar 

  21. Dawson-Hughes B, Harris SS, Rasmussen HM, Dallal GE (2007) Comparative effects of oral aromatic and branched-chain amino acids on urine calcium excretion in humans. Osteoporos Int 18(7):955–961. doi:10.1007/s00198-006-0320-x

    Article  CAS  PubMed  Google Scholar 

  22. Kerstetter JE, Mitnick ME, Gundberg CM, Caseria DM, Ellison AF, Carpenter TO, Insogna KL (1999) Changes in bone turnover in young women consuming different levels of dietary protein. J Clin Endocrinol Metab 84(3):1052–1055. doi:10.1210/jcem.84.3.5552

    CAS  PubMed  Google Scholar 

  23. Rozenberg S, Body JJ, Bruyere O, Bergmann P, Brandi ML, Cooper C, Devogelaer JP, Gielen E, Goemaere S, Kaufman JM, Rizzoli R, Reginster JY (2016) Effects of dairy products consumption on health: benefits and beliefs–a commentary from the Belgian Bone Club and the European Society for clinical and economic aspects of osteoporosis, osteoarthritis and musculoskeletal diseases. Calcif Tissue Int 98(1):1–17. doi:10.1007/s00223-015-0062-x

    Article  CAS  PubMed  Google Scholar 

  24. 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. doi:10.1002/jbmr.279

    Article  CAS  PubMed  Google Scholar 

  25. Feskanich D, Bischoff-Ferrari HA, Frazier AL, Willett WC (2014) Milk consumption during teenage years and risk of hip fractures in older adults. JAMA Pediatr 168(1):54–60. doi:10.1001/jamapediatrics.2013.3821

    Article  PubMed  PubMed Central  Google Scholar 

  26. 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. doi:10.1007/s00198-016-3898-7

    Article  CAS  PubMed  Google Scholar 

  27. 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. doi:10.1007/s11657-013-0119-2

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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  Google Scholar 

  29. 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. doi:10.1002/jbmr.2896

    Article  CAS  PubMed  Google Scholar 

  30. de Jonge EA, Kiefte-de Jong JC (2017) Dietary patterns explaining differences in bone mineral density and hip structure in the elderly: the Rotterdam Study. Am J Clin Nutr 105(1):203–211. doi:10.3945/ajcn.116.139196

    Article  PubMed  Google Scholar 

  31. Adolphi B, Scholz-Ahrens KE, de Vrese M, Acil Y, Laue C, Schrezenmeir J (2009) Short-term effect of bedtime consumption of fermented milk supplemented with calcium, inulin-type fructans and caseinphosphopeptides on bone metabolism in healthy, postmenopausal women. Eur J Nutr 48(1):45–53. doi:10.1007/s00394-008-0759-y

    Article  CAS  PubMed  Google Scholar 

  32. Kruger MC, Chan YM, Kuhn-Sherlock B, Lau LT, Lau C, Chin YS, Todd JM, Schollum LM (2016) Differential effects of calcium- and vitamin D-fortified milk with FOS-inulin compared to regular milk, on bone biomarkers in Chinese pre- and postmenopausal women. Eur J Nutr 55(5):1911–1921. doi:10.1007/s00394-015-1007-x

    Article  CAS  PubMed  Google Scholar 

  33. Narva M, Nevala R, Poussa T, Korpela R (2004) The effect of Lactobacillus helveticus fermented milk on acute changes in calcium metabolism in postmenopausal women. Eur J Nutr 43(2):61–68. doi:10.1007/s00394-004-0441-y

    Article  CAS  PubMed  Google Scholar 

  34. Chan GM, Hoffman K, McMurry M (1995) Effects of dairy products on bone and body composition in pubertal girls. J Pediatr 126(4):551–556

    Article  CAS  PubMed  Google Scholar 

  35. Merrilees MJ, Smart EJ, Gilchrist NL, Frampton C, Turner JG, Hooke E, March RL, Maguire P (2000) Effects of diary food supplements on bone mineral density in teenage girls. Eur J Nutr 39(6):256–262

    Article  CAS  PubMed  Google Scholar 

  36. He M, Yang YX, Han H, Men JH, Bian LH, Wang GD (2005) Effects of yogurt supplementation on the growth of preschool children in Beijing suburbs. Biomed Environ Sci 18(3):192–197

    PubMed  Google Scholar 

  37. Cheng S, Lyytikainen A, Kroger H, Lamberg-Allardt C, Alen M, Koistinen A, Wang QJ, Suuriniemi M, Suominen H, Mahonen A, Nicholson PH, Ivaska KK, Korpela R, Ohlsson C, Vaananen KH, Tylavsky F (2005) Effects of calcium, dairy product, and vitamin D supplementation on bone mass accrual and body composition in 10-12-y-old girls: a 2-y randomized trial. Am J Clin Nutr 82(5):1115–1126 quiz 1147–1118

    Article  CAS  PubMed  Google Scholar 

  38. Manios Y, Moschonis G, Trovas G, Lyritis GP (2007) Changes in biochemical indexes of bone metabolism and bone mineral density after a 12-mo dietary intervention program: the Postmenopausal Health Study. Am J Clin Nutr 86(3):781–789

    Article  CAS  PubMed  Google Scholar 

  39. Manios Y, Moschonis G, Koutsikas K, Papoutsou S, Petraki I, Bellou E, Naoumi A, Kostea S, Tanagra S (2009) Changes in body composition following a dietary and lifestyle intervention trial: the postmenopausal health study. Maturitas 62(1):58–65. doi:10.1016/j.maturitas.2008.11.005

    Article  PubMed  Google Scholar 

  40. Bonjour JP, Benoit V, Pourchaire O, Rousseau B, Souberbielle JC (2011) Nutritional approach for inhibiting bone resorption in institutionalized elderly women with vitamin D insufficiency and high prevalence of fracture. J Nutr Health Aging 15(5):404–409

    Article  CAS  PubMed  Google Scholar 

  41. Bonjour JP, Benoit V, Rousseau B, Souberbielle JC (2012) Consumption of vitamin D-and calcium-fortified soft white cheese lowers the biochemical marker of bone resorption TRAP 5b in postmenopausal women at moderate risk of osteoporosis fracture. J Nutr 142(4):698–703. doi:10.3945/jn.111.153692

    Article  CAS  PubMed  Google Scholar 

  42. Trombetti A, Carrier E, Perroud A, Lang F, Herrmann FR, Rizzoli R (2016) Influence of a fermented protein-fortified dairy product on serum insulin-like growth factor-I in women with anorexia nervosa: a randomized controlled trial. Clin Nutr 35(5):1032–1038. doi:10.1016/j.clnu.2015.10.014

    Article  CAS  PubMed  Google Scholar 

  43. Heaney RP, Rafferty K, Dowell MS (2002) Effect of yogurt on a urinary marker of bone resorption in postmenopausal women. J Am Diet Assoc 102(11):1672–1674

    Article  PubMed  Google Scholar 

  44. Tenta R, Moschonis G, Koutsilieris M, Manios Y (2011) Calcium and vitamin D supplementation through fortified dairy products counterbalances seasonal variations of bone metabolism indices: the Postmenopausal Health Study. Eur J Nutr 50(5):341–349. doi:10.1007/s00394-010-0142-7

    Article  CAS  PubMed  Google Scholar 

  45. Bonjour JP, Benoit V, Payen F, Kraenzlin M (2013) Consumption of yogurts fortified in vitamin D and calcium reduces serum parathyroid hormone and markers of bone resorption: a double-blind randomized controlled trial in institutionalized elderly women. J Clin Endocrinol Metab 98(7):2915–2921. doi:10.1210/jc.2013-1274

    Article  CAS  PubMed  Google Scholar 

  46. Jafari T, Faghihimani E, Feizi A, Iraj B, Javanmard SH, Esmaillzadeh A, Fallah AA, Askari G (2016) Effects of vitamin D-fortified low fat yogurt on glycemic status, anthropometric indexes, inflammation, and bone turnover in diabetic postmenopausal women: a randomised controlled clinical trial. Clin Nutr 35(1):67–76. doi:10.1016/j.clnu.2015.02.014

    Article  CAS  PubMed  Google Scholar 

  47. Bonjour JP, Benoit V, Atkin S, Walrand S (2015) Fortification of yogurts with vitamin D and calcium enhances the inhibition of serum parathyroid hormone and bone resorption markers: a double blind randomized controlled trial in women over 60 living in a community dwelling home. J Nutr Health Aging 19(5):563–569. doi:10.1007/s12603-015-0498-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Neyestani TR, Nikooyeh B, Kalayi A, Zahedirad M, Shariatzadeh N (2015) A vitamin D-calcium-fortified yogurt drink decreased serum PTH but did not affect osteocalcin in subjects with Type 2 diabetes. Int J Vitam Nutr Res 85(1–2):61–69. doi:10.1024/0300-9831/a000227

    Article  CAS  PubMed  Google Scholar 

  49. Bonjour JP, Benoit V, Pourchaire 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(7):962–966. doi:10.1017/s0007114509371743

    Article  CAS  PubMed  Google Scholar 

  50. Moschonis G, Manios Y (2006) Skeletal site-dependent response of bone mineral density and quantitative ultrasound parameters following a 12-month dietary intervention using dairy products fortified with calcium and vitamin D: the Postmenopausal Health Study. Br J Nutr 96(6):1140–1148

    Article  CAS  PubMed  Google Scholar 

  51. Moschonis G, Katsaroli I, Lyritis GP, Manios Y (2010) The effects of a 30-month dietary intervention on bone mineral density: the Postmenopausal Health Study. Br J Nutr 104(1):100–107. doi:10.1017/s000711451000019x

    Article  CAS  PubMed  Google Scholar 

  52. Moschonis G, Kanellakis S, Papaioannou N, Schaafsma A, Manios Y (2011) Possible site-specific effect of an intervention combining nutrition and lifestyle counselling with consumption of fortified dairy products on bone mass: the Postmenopausal Health Study II. J Bone Miner Metab 29(4):501–506. doi:10.1007/s00774-010-0256-2

    Article  CAS  PubMed  Google Scholar 

  53. Rizzoli R, Bischoff-Ferrari H, Dawson-Hughes B, Weaver C (2014) Nutrition and bone health in women after the menopause. Womens Health (Lond) 10(6):599–608. doi:10.2217/whe.14.40

    Article  CAS  Google Scholar 

  54. Fenton TR, Tough SC, Lyon AW, Eliasziw M, Hanley DA (2011) Causal assessment of dietary acid load and bone disease: a systematic review & meta-analysis applying Hill’s epidemiologic criteria for causality. Nutr J 10:41. doi:10.1186/1475-2891-10-41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Shams-White MM, Chung M, Du M, Fu Z, Insogna KL, Karlsen MC, LeBoff MS, Shapses SA, Sackey J, Wallace TC, Weaver CM (2017) Dietary protein and bone health: a systematic review and meta-analysis from the National Osteoporosis Foundation. Am J Clin Nutr 105(6):1528–1543. doi:10.3945/ajcn.116.145110

    CAS  PubMed  Google Scholar 

  56. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, Wolvers D, Watzl B, Szajewska H, Stahl B, Guarner F, Respondek F, Whelan K, Coxam V, Davicco MJ, Leotoing L, Wittrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A (2010) Prebiotic effects: metabolic and health benefits. Br J Nutr 104(Suppl 2):S1–S63. doi:10.1017/s0007114510003363

    Article  CAS  PubMed  Google Scholar 

  57. He Y, Liu S, Leone S, Newburg DS (2014) Human colostrum oligosaccharides modulate major immunologic pathways of immature human intestine. Mucosal Immunol 7(6):1326–1339. doi:10.1038/mi.2014.20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Charbonneau MR, O’Donnell D, Blanton LV, Totten SM, Davis JC, Barratt MJ, Cheng J, Guruge J, Talcott M, Bain JR, Muehlbauer MJ, Ilkayeva O, Wu C, Struckmeyer T, Barile D, Mangani C, Jorgensen J, Fan YM, Maleta K, Dewey KG, Ashorn P, Newgard CB, Lebrilla C, Mills DA, Gordon JI (2016) Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 164(5):859–871. doi:10.1016/j.cell.2016.01.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, Subramanian S, Manary MJ, Trehan I, Jorgensen JM, Fan YM, Henrissat B, Leyn SA, Rodionov DA, Osterman AL, Maleta KM, Newgard CB, Ashorn P, Dewey KG, Gordon JI (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. doi:10.1126/science.aad3311

    PubMed Central  Google Scholar 

  60. Ammann P, Rizzoli R, Fleisch H (1988) Influence of the disaccharide lactitol on intestinal absorption and body retention of calcium in rats. J Nutr 118(6):793–795

    Article  CAS  PubMed  Google Scholar 

  61. Weaver CM, Martin BR, Nakatsu CH, Armstrong AP, Clavijo A, McCabe LD, McCabe GP, Duignan S, Schoterman MH, van den Heuvel EG (2011) Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. J Agric Food Chem 59(12):6501–6510. doi:10.1021/jf2009777

    Article  CAS  PubMed  Google Scholar 

  62. Mathewson ND, Jenq R, Mathew AV, Koenigsknecht M, Hanash A, Toubai T, Oravecz-Wilson K, Wu SR, Sun Y, Rossi C, Fujiwara H, Byun J, Shono Y, Lindemans C, Calafiore M, Schmidt TC, Honda K, Young VB, Pennathur S, van den Brink M, Reddy P (2016) Gut microbiome-derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versus-host disease. Nat Immunol 17(5):505–513. doi:10.1038/ni.3400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Matthies A, Loh G, Blaut M, Braune A (2012) Daidzein and genistein are converted to equol and 5-hydroxy-equol by human intestinal Slackia isoflavoniconvertens in gnotobiotic rats. J Nutr 142(1):40–46. doi:10.3945/jn.111.148247

    Article  CAS  PubMed  Google Scholar 

  64. Peng L, Li ZR, Green RS, Holzman IR, Lin J (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 139(9):1619–1625. doi:10.3945/jn.109.104638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Abrams SA, Griffin IJ, Hawthorne KM, Liang L, Gunn SK, Darlington G, Ellis KJ (2005) A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr 82(2):471–476

    Article  CAS  PubMed  Google Scholar 

  66. Holloway L, Moynihan S, Abrams SA, Kent K, Hsu AR, Friedlander AL (2007) Effects of oligofructose-enriched inulin on intestinal absorption of calcium and magnesium and bone turnover markers in postmenopausal women. Br J Nutr 97(2):365–372. doi:10.1017/s000711450733674x

    Article  CAS  PubMed  Google Scholar 

  67. McNulty NP, Yatsunenko T, Hsiao A, Faith JJ, Muegge BD, Goodman AL, Henrissat B, Oozeer R, Cools-Portier S, Gobert G, Chervaux C, Knights D, Lozupone CA, Knight R, Duncan AE, Bain JR, Muehlbauer MJ, Newgard CB, Heath AC, Gordon JI (2011) The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 3(106):106ra106. doi:10.1126/scitranslmed.3002701

  68. Alvaro E, Andrieux C, Rochet V, Rigottier-Gois L, Lepercq P, Sutren M, Galan P, Duval Y, Juste C, Dore J (2007) Composition and metabolism of the intestinal microbiota in consumers and non-consumers of yogurt. Br J Nutr 97(1):126–133. doi:10.1017/s0007114507243065

    Article  CAS  PubMed  Google Scholar 

  69. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome (2012). Nature 486(7402):207–214. doi:10.1038/nature11234

    Article  Google Scholar 

  70. Mineo H, Amano M, Minaminida K, Chiji H, Shigematsu N, Tomita F, Hara H (2006) Two-week feeding of difructose anhydride III enhances calcium absorptive activity with epithelial cell proliferation in isolated rat cecal mucosa. Nutrition 22(3):312–320. doi:10.1016/j.nut.2005.06.015

    Article  CAS  PubMed  Google Scholar 

  71. Ross AB, Pere-Trepat E, Montoliu I, Martin FP, Collino S, Moco S, Godin JP, Cleroux M, Guy PA, Breton I, Bibiloni R, Thorimbert A, Tavazzi I, Tornier L, Bebuis A, Bruce SJ, Beaumont M, Fay LB, Kochhar S (2013) A whole-grain-rich diet reduces urinary excretion of markers of protein catabolism and gut microbiota metabolism in healthy men after one week. J Nutr 143(6):766–773. doi:10.3945/jn.112.172197

    Article  CAS  PubMed  Google Scholar 

  72. Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, Bultman SJ (2011) The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13(5):517–526. doi:10.1016/j.cmet.2011.02.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Backhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27(6):1357–1367. doi:10.1002/jbmr.1588

    Article  PubMed  PubMed Central  Google Scholar 

  74. Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, Schutz G, Glorieux FH, Chiang CY, Zajac JD, Insogna KL, Mann JJ, Hen R, Ducy P, Karsenty G (2008) Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135(5):825–837. doi:10.1016/j.cell.2008.09.059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Li JY, Tawfeek H, Bedi B, Yang X, Adams J, Gao KY, Zayzafoon M, Weitzmann MN, Pacifici R (2011) Ovariectomy disregulates osteoblast and osteoclast formation through the T-cell receptor CD40 ligand. Proc Natl Acad Sci USA 108(2):768–773. doi:10.1073/pnas.1013492108

    Article  CAS  PubMed  Google Scholar 

  76. Macpherson AJ, Uhr T (2004) Compartmentalization of the mucosal immune responses to commensal intestinal bacteria. Ann N Y Acad Sci 1029:36–43. doi:10.1196/annals.1309.005

    Article  CAS  PubMed  Google Scholar 

  77. Li JY, Chassaing B, Tyagi AM, Vaccaro C, Luo T, Adams J, Darby TM, Weitzmann MN, Mulle JG, Gewirtz AT, Jones RM, Pacifici R (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126(6):2049–2063. doi:10.1172/jci86062

    Article  PubMed  PubMed Central  Google Scholar 

  78. Iqbal J, Yuen T, Sun L, Zaidi M (2016) From the gut to the strut: where inflammation reigns, bone abstains. J Clin Invest 126(6):2045–2048. doi:10.1172/jci87430

    Article  PubMed  PubMed Central  Google Scholar 

  79. Ohlsson C, Engdahl C, Fak F, Andersson A, Windahl SH, Farman HH, Moverare-Skrtic S, Islander U, Sjogren K (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE 9(3):e92368. doi:10.1371/journal.pone.0092368

    Article  PubMed  PubMed Central  Google Scholar 

  80. Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229(11):1822–1830. doi:10.1002/jcp.24636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. McCabe LR, Irwin R, Schaefer L, Britton RA (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 228(8):1793–1798. doi:10.1002/jcp.24340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Lotters FJ, Lenoir-Wijnkoop I, Fardellone P, Rizzoli R, Rocher E, Poley MJ (2013) Dairy foods and osteoporosis: an example of assessing the health-economic impact of food products. Osteoporos Int 24(1):139–150. doi:10.1007/s00198-012-1998-6

    Article  CAS  PubMed  Google Scholar 

  83. Ethgen O, Hiligsmann M, Burlet N, Reginster JY (2016) Cost-effectiveness of personalized supplementation with vitamin D-rich dairy products in the prevention of osteoporotic fractures. Osteoporos Int 27(1):301–308. doi:10.1007/s00198-015-3319-3

    Article  CAS  PubMed  Google Scholar 

  84. 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. doi:10.3945/ajcn.115.123216

    Article  CAS  PubMed  Google Scholar 

  85. USDA National Nutrient Database for Standard Reference. Release 28. 2015 http://ndb.nal.usda.gov/ndb/nutrients/index

  86. Brett NR, Lavery P, Agellon S, Vanstone CA, Maguire JL, Rauch F, Weiler HA (2016) Dietary vitamin D dose-response in healthy children 2 to 8 y of age: a 12-wk randomized controlled trial using fortified foods. Am J Clin Nutr 103(1):144–152. doi:10.3945/ajcn.115.115956

    Article  CAS  PubMed  Google Scholar 

  87. Tu MY, Chen HL, Tung YT, Kao CC, Hu FC, Chen CM (2015) Short-term effects of kefir-fermented milk consumption on bone mineral density and bone metabolism in a randomized clinical trial of osteoporotic patients. PLoS ONE 10(12):e0144231. doi:10.1371/journal.pone.0144231

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Conflict of interest

René Rizzoli received fees from Danone, Nestlé, and CNIEL for lectures or advisory boards. Emmanuel Biver received a grant from Danone for a research project.

Author information

Authors and Affiliations

  1. Service of Bone Diseases, Faculty of Medicine, Geneva University Hospitals, 1211, Geneva 14, Switzerland

    René Rizzoli & Emmanuel Biver

Authors
  1. René Rizzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmanuel Biver
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to René Rizzoli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rizzoli, R., Biver, E. Effects of Fermented Milk Products on Bone. Calcif Tissue Int 102, 489–500 (2018). https://doi.org/10.1007/s00223-017-0317-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-017-0317-9

Keywords

Search

Navigation