Skip to main content

Advertisement

SpringerLink
Log in

Influence of High and Low Protein Intakes on Age-Related Bone Loss in Rats Submitted to Adequate or Restricted Energy Conditions

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Low energy and protein intake has been suggested to contribute to the increased incidence of osteoporosis in the elderly. The impact of dietary protein on bone health is still a matter of debate. Therefore, we examined the effect of the modulation of protein intake under adequate or deficient energy conditions on bone status in 16-month-old male rats. The animals were randomly allocated to six groups (n = 10/group). Control animals were fed a diet providing either a normal-protein content (13%, C-NP) or a high-protein content (26%) (C-HP). The other groups received a 40% protein/energy–restricted diet (PER-NP and PER-HP) or a normal protein/energy–restricted diet (ER-NP and ER-HP). After 5 months of the experiment, protein intake (13% or 26%) did not modulate calcium retention or bone status in those rats, although a low-grade metabolic acidosis was induced with the HP diet. Both restrictions (PER and ER) decreased femoral bone mineral density and fracture load. Plasma osteocalcin and urinary deoxypyridinoline levels were lowered, suggesting a decrease in bone turnover in the PER and ER groups. Circulating insulin-like growth factor-I levels were also lowered by dietary restrictions, together with calcium retention. Adequate protein intake in the ER condition did not elicit any bone-sparing effect compared to PER rats. In conclusion, both energy and protein deficiencies may contribute to age-related bone loss. This study highlights the importance of sustaining adequate energy and protein provision to preserve skeletal integrity in the elderly.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761–1767

    Article  PubMed  Google Scholar 

  2. Wilkins CH, Birge SJ (2005) Prevention of osteoporotic fractures in the elderly. Am J Med 118:1190–1195

    Article  PubMed  Google Scholar 

  3. Bonjour J, Schürch MA, Rizzoli R (1997) Nutritional aspects of hip fractures. Bone 18(3 Suppl):139S–144S

    Google Scholar 

  4. Ilich JZ, Kerstetter JE (2000) Nutrition in bone health revisited: a story beyond calcium. J Am Coll Nutr 19:715–737

    PubMed  CAS  Google Scholar 

  5. Hannan MT, Tucker KL, Dawson-Hughes B, Cupples LA, Felson DT, Kiel DP (2000) Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:2504–2512

    Article  PubMed  CAS  Google Scholar 

  6. Devine A, Dick IM, Islam AF, Dhaliwal SS, Prince RL (2005) Protein consumption is an important predictor of lower limb bone mass in elderly women. Am J Clin Nutr 81:1423–1428

    PubMed  Google Scholar 

  7. Coin A, Sergi G, Beninca P, Lupoli L, Cinti G, Ferrara L, Benedetti G, Tomasi G, Pisent C, Enzi G (2000) Bone mineral density and body composition in underweight and normal elderly subjects. Osteoporos Int 11:1043–1050

    Article  PubMed  CAS  Google Scholar 

  8. Delmi M, Rapin CH, Bengoa JM, Delmas PD, Vasey H, Bonjour JP (1990) Dietary supplementation in elderly patients with fractured neck of the femur. Lancet 335:1013–1016

    Article  PubMed  CAS  Google Scholar 

  9. Schurch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P, Bonjour JP (1998) Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 128:801–809

    PubMed  CAS  Google Scholar 

  10. Mardon J, Zangarelli A, Walrand S, Davicco MJ, Lebecque P, Demigné C, Horcajada MN, Boirie Y, Coxam V (2008) Impact of energy and casein or whey protein intake on bone status in a rat model of age-related bone loss. Br J Nutr 99(4):764–772

    Article  PubMed  CAS  Google Scholar 

  11. Sanderson JP, Binkley N, Roecker EB, Champ JE, Pugh TD, Aspnes L, Weindruch R (1997) Influence of fat intake and caloric restriction on bone in aging male rats. J Gerontol A Biol Sci Med Sci 52:B20–B25

    PubMed  CAS  Google Scholar 

  12. Talbott SM, Cifuentes M, Dunn MG, Shapses SA (2001) Energy restriction reduces bone density and biomechanical properties in aged female rats. J Nutr 131:2382–2387

    PubMed  CAS  Google Scholar 

  13. Lee C, Panemangalore M, Wilson K (1986) Effect of dietary energy restriction on bone mineral content of mature rats. Nutr Res 6:51–59

    Article  CAS  Google Scholar 

  14. LaMothe JM, Hepple RT, Zernicke RF (2003) Bone adaptation with aging and long-term caloric restriction in Fischer 344 x Brown-Norway F1-hybrid rats. J Appl Physiol 95:1739–1745

    PubMed  Google Scholar 

  15. Bourrin S, Toromanoff A, Ammann P, Bonjour JP, Rizzoli R (2000) Dietary protein deficiency induces osteoporosis in aged male rats. J Bone Miner Res 15:1555–1563

    Article  PubMed  CAS  Google Scholar 

  16. Ammann P, Laib A, Bonjour JP, Meyer JM, Ruegsegger P, Rizzoli R (2002) Dietary essential amino acid supplements increase bone strength by influencing bone mass and bone microarchitecture in ovariectomized adult rats fed an isocaloric low-protein diet. J Bone Miner Res 17:1264–1272

    Article  PubMed  CAS  Google Scholar 

  17. Promislow JH, Goodman-Gruen D, Slymen DJ, Barrett-Connor E (2002) Protein consumption and bone mineral density in the elderly: the Rancho Bernardo Study. Am J Epidemiol 155:636–644

    Article  PubMed  Google Scholar 

  18. Kerstetter JE, O’Brien KO, Caseria DM, Wall DE, Insogna KL (2005) The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab 90:26–31

    Article  PubMed  CAS  Google Scholar 

  19. Dawson-Hughes B, Harris SS, Rasmussen H, Song L, Dallal GE (2004) Effect of dietary protein supplements on calcium excretion in healthy older men and women. J Clin Endocrinol Metab 89:1169–1173

    Article  PubMed  CAS  Google Scholar 

  20. Thissen JP, Ketelslegers JM, Underwood LE (1994) Nutritional regulation of the insulin-like growth factors. Endocr Rev 15:80–101

    Article  PubMed  CAS  Google Scholar 

  21. Clemmons DR, Underwood LE (1991) Nutritional regulation of IGF-I and IGF binding proteins. Annu Rev Nutr 11:393–412

    Article  PubMed  CAS  Google Scholar 

  22. Chan EL, Swaminathan R (1994) The effect of high protein and high salt intake for 4 months on calcium and hydroxyproline excretion in normal and oophorectomized rats. J Lab Clin Med 124:37–41

    PubMed  CAS  Google Scholar 

  23. Amanzadeh J, Gitomer WL, Zerwekh JE, Preisig PA, Moe OW, Pak CY, Levi M (2003) Effect of high protein diet on stone-forming propensity and bone loss in rats. Kidney Int 64:2142–2149

    Article  PubMed  CAS  Google Scholar 

  24. Arnett T (2007) Acid-base regulation of bone metabolism. Int Congr Series 1297:255–267

    Article  CAS  Google Scholar 

  25. Krieger NS, Frick KK, Bushinsky DA (2004) Mechanism of acid-induced bone resorption. Curr Opin Nephrol Hypertens 13:423–436

    Article  PubMed  CAS  Google Scholar 

  26. Zwart SR, Davis-Street JE, Paddon-Jones D, Ferrando AA, Wolfe RR, Smith SM (2005) Amino acid supplementation alters bone metabolism during simulated weightlessness. J Appl Physiol 99:134–140

    Article  PubMed  CAS  Google Scholar 

  27. Feskanich D, Willett WC, Stampfer MJ, Colditz GA (1996) Protein consumption and bone fractures in women. Am J Epidemiol 143:472–479

    PubMed  CAS  Google Scholar 

  28. Pugh TD, Klopp RG, Weindruch R (1999) Controlling caloric consumption: protocols for rodents and rhesus monkeys. Neurobiol Aging 20:157–165

    Article  PubMed  CAS  Google Scholar 

  29. Colwell A, Russell RG, Eastell R (1993) Factors affecting the assay of urinary 3-hydroxy pyridinium crosslinks of collagen as markers of bone resorption. Eur J Clin Invest 23:341–349

    Article  PubMed  CAS  Google Scholar 

  30. Omi N, Ezawa I (1995) The effect of ovariectomy on bone metabolism in rats. Bone 17:163S–168S

    PubMed  CAS  Google Scholar 

  31. Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608

    Article  PubMed  CAS  Google Scholar 

  32. Lane MA, Black A, Handy AM, Shapses SA, Tilmont EM, Kiefer TL, Ingram DK, Roth GS (2001) Energy restriction does not alter bone mineral metabolism or reproductive cycling and hormones in female rhesus monkeys. J Nutr 131:820–827

    PubMed  CAS  Google Scholar 

  33. Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S et al (1995) Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1:1155–1161

    Article  PubMed  CAS  Google Scholar 

  34. Schapira D, Lotan-Miller R, Barzilai D, Silbermann M (1991) The rat as a model for studies of the aging skeleton. Cells Materials Suppl 1:181–188

    Google Scholar 

  35. Talbott SM, Rothkopf MM, Shapses SA (1998) Dietary restriction of energy and calcium alters bone turnover and density in younger and older female rats. J Nutr 128:640–645

    PubMed  CAS  Google Scholar 

  36. Brochmann Murray EJ, Beamer WG, Duarte ME, Behnam K, Grisanti MS, Murray SS (2001) Effects of dietary restriction on appendicular bone in the SENCAR mouse. Metabolism 50:436–442

    Article  PubMed  CAS  Google Scholar 

  37. Kalu DN, Hardin RR, Cockerham R, Yu BP, Norling BK, Egan JW (1984) Lifelong food restriction prevents senile osteopenia and hyperparathyroidism in F344 rats. Mech Ageing Dev 26:103–112

    Article  PubMed  CAS  Google Scholar 

  38. Black A, Allison DB, Shapses SA, Tilmont EM, Handy AM, Ingram DK, Roth GS, Lane MA (2001) Calorie restriction and skeletal mass in rhesus monkeys (Macaca mulatta): evidence for an effect mediated through changes in body size. J Gerontol A Biol Sci Med Sci 56:B98–B107

    PubMed  CAS  Google Scholar 

  39. Lemann J Jr (1999) Relationship between urinary calcium and net acid excretion as determined by dietary protein and potassium: a review. Nephron 81(Suppl 1):18–25

    Article  PubMed  CAS  Google Scholar 

  40. Allen LH, Hall TE (1978) Calcium metabolism, intestinal calcium-binding protein, and bone growth of rats fed high protein diets. J Nutr 108:967–972

    PubMed  CAS  Google Scholar 

  41. Sabboh H, Horcajada MN, Coxam V, Tressol JC, Besson C, Remesy C, Demigne C (2005) Effect of potassium salts in rats adapted to an acidogenic high-sulfur amino acid diet. Br J Nutr 94:192–197

    Article  PubMed  CAS  Google Scholar 

  42. Breslau NA, Brinkley L, Hill KD, Pak CY (1988) Relationship of animal protein-rich diet to kidney stone formation and calcium metabolism. J Clin Endocrinol Metab 66:140–146

    Article  PubMed  CAS  Google Scholar 

  43. Brennan TS, Klahr S, Hamm LL (1986) Citrate transport in rabbit nephron. Am J Physiol Renal Physiol 251:F683–F689

    CAS  Google Scholar 

  44. Labow BI, Souba WW, Abcouwer SF (2001) Mechanisms governing the expression of the enzymes of glutamine metabolism—glutaminase and glutamine synthetase. J Nutr 131:2467S–2474S, 2486S

    PubMed  CAS  Google Scholar 

  45. Nakamura H, Kajikawa R, Ubuka T (2002) A study on the estimation of sulfur-containing amino acid metabolism by the determination of urinary sulfate and taurine. Amino Acids 23:427–431

    Article  PubMed  CAS  Google Scholar 

  46. Sabboh H, Coxam V, Horcajada MN, Remesy C, Demigne C (2007) Effects of plant food potassium salts (citrate, galacturonate or tartrate) on acid-base status and digestive fermentations in rats. Br J Nutr 98:72–77

    Article  PubMed  CAS  Google Scholar 

  47. Krieger NS, Sessler NE, Bushinsky DA (1992) Acidosis inhibits osteoblastic and stimulates osteoclastic activity in vitro. Am J Physiol Renal Physiol 262:F442–F448

    CAS  Google Scholar 

  48. Arnett T (2003) Regulation of bone cell function by acid-base balance. Proc Nutr Soc 62:511–520

    Article  PubMed  CAS  Google Scholar 

  49. Goulding A, Campbell DR (1984) Effects of oral loads of sodium chloride on bone composition in growing rats consuming ample dietary calcium. Miner Electrolyte Metab 10:58–62

    PubMed  CAS  Google Scholar 

  50. Creedon A, Cashman KD (2000) The effect of high salt and high protein intake on calcium metabolism, bone composition and bone resorption in the rat. Br J Nutr 84:49–56

    PubMed  CAS  Google Scholar 

  51. Whiting SJ, Draper HH (1981) Effect of chronic high protein feeding on bone composition in the adult rat. J Nutr 111:178–183

    PubMed  CAS  Google Scholar 

  52. Calvo MS, Bell RR, Forbes RM (1982) Effect of protein-induced calciuria on calcium metabolism and bone status in adult rats. J Nutr 112:1401–1413

    PubMed  CAS  Google Scholar 

  53. Zernicke RF, Salem GJ, Barnard RJ, Woodward JS Jr, Meduski JW, Meduski JD (1995) Adaptations of immature trabecular bone to exercise and augmented dietary protein. Med Sci Sports Exerc 27:1486–1493

    PubMed  CAS  Google Scholar 

  54. 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

    PubMed  CAS  Google Scholar 

  55. Bonjour JP, Ammann P, Chevalley T, Rizzoli R (2001) Protein intake and bone growth. Can J Appl Physiol 26(Suppl):S153–S166

    PubMed  CAS  Google Scholar 

  56. Ndiaye B, Cournot G, Pelissier MA, Debray OW, Lemonnier D (1995) Rat serum osteocalcin concentration is decreased by restriction of energy intake. J Nutr 125:1283–1290

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unité de Nutrition Humaine UMR1019, Institut National de la Recherche Agronomique Clermont-Ferrand/Theix, 63122, Saint Genes Champanelle, France

    Julie Mardon, Véronique Habauzit, Anna Trzeciakiewicz, Marie-Jeanne Davicco, Patrice Lebecque, Sylvie Mercier, Jean-Claude Tressol, Marie-Noëlle Horcajada, Christian Demigné & Véronique Coxam

Authors
  1. Julie Mardon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Véronique Habauzit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna Trzeciakiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marie-Jeanne Davicco
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patrice Lebecque
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sylvie Mercier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jean-Claude Tressol
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marie-Noëlle Horcajada
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christian Demigné
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Véronique Coxam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julie Mardon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mardon, J., Habauzit, V., Trzeciakiewicz, A. et al. Influence of High and Low Protein Intakes on Age-Related Bone Loss in Rats Submitted to Adequate or Restricted Energy Conditions. Calcif Tissue Int 82, 373–382 (2008). https://doi.org/10.1007/s00223-008-9125-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-008-9125-6

Keywords

Search

Navigation