Skip to main content

Advertisement

SpringerLink
Log in

Low Protein Intake Magnifies Detrimental Effects of Ovariectomy and Vitamin D on Bone

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Protein-induced changes in bone and calcium homeostasis could potentially be greater in the elderly and in women at risk for osteoporosis. We hypothesize that a low protein intake would magnify the negative changes in bone metabolism seen in vitamin D (vitD) insufficiency and/or estrogen deficiency. The present study was undertaken to better understand how a low protein diet along with vitD insufficiency could affect bone metabolism using a rodent ovariectomized (OVX) model. Rats (n = 60) underwent ovariectomy (OVX) or sham operation. The first 15 days after surgery, all rats were fed a standard rodent diet. Thereafter, rats (n = 10/group) were fed a low protein diet (LP; 2.5 %) or a control diet (NP; 12.5 %) with 100 IU% vitD (+D; cholecalciferol) or without vitD (−D) for 45 days. The groups were as follows: SHAM + NP + D (control); SHAM + LP + D; SHAM + LP − D; OVX + NP + D; OVX + LP + D; OVX + LP − D. Body weight (BW) of control and OVX + NP + D groups increased while those feeding the LP diet, independently of vitD feedings, decreased (p < 0.05). The OVX + LP − D group presented the lowest serum Ca, phosphorus and osteocalcin levels and the highest CTX levels (p < 0.05). At the end of the study, total skeleton bone mineral content, proximal tibia bone mineral density, bone volume and trabecular number levels decreased as follows: SHAM + NP + D (controls) > SHAM + LP + D > OVX + NP + D > SHAM + LP − D > OVX + LP + D > OVX + LP − D (p < 0.05). A low protein diet negatively affected bone mass and magnified the detrimental effects of vitD and/or estrogen deficiencies.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Heaney RP (2007) Effects of protein on the calcium economy. In: Burckhardt P, Heaney RP, Dawson-Hughes B (eds) Nutritional aspects of osteoporosis. Elsevier, Amsterdam, pp 191–197

    Google Scholar 

  2. Kerstetter JE, O’Brien KO, Insogna KL (2003) Dietary protein, calcium metabolism, and skeletal homeostasis revisited. Am J Clin Nutr 78(Suppl 1):584S–592S

    PubMed  CAS  Google Scholar 

  3. Welten DC, Kemper HCG, Post GB, van Stavaren WAA (1995) A meta-analysis of the effects of calcium intake on bone mass in young and middle aged females and males. J Nutr 125:2802–2813

    PubMed  CAS  Google Scholar 

  4. Shea B, Wells G, Cranney A, Zytaruk N, Robinson V, Griffith L, Ortiz Z, Peterson J, Adachi J, Tugwell P, Guyatt G (2002) Meta-analyses of therapies for postmenopausal osteoporosis. VII. Meta-analysis of calcium supplementation for the prevention of postmenopausal osteoporosis. Endocr Rev 23:552–559

    Article  PubMed  CAS  Google Scholar 

  5. Reginster JY (2005) The high prevalence of inadequate serum vitamin D levels and implications for bone health. Curr Med Res Opin 21:579–586

    Article  PubMed  CAS  Google Scholar 

  6. Gordon CM, DePeter KC, Feldman HA, Grace E, Emans SJ (2004) Prevalence of vitamin D deficiency among healthy adolescents. Arch Pediatr Adolesc Med 158:531–537

    Article  PubMed  Google Scholar 

  7. Lehtonen-Veromaa MK, Mottonen TT, Nuotio IO, Irjala KM, Leino AE, Viikari JS (2002) Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: a 3-y prospective study. Am J Clin Nutr 76:1446–1453

    PubMed  CAS  Google Scholar 

  8. Steingrimsdottir L, Gunnarsson O, Indridason OS, Franzson L, Sigurdsson G (2005) Relationship between serum parathyroid hormone levels, vitamin D sufficiency, and calcium intake. JAMA 294:2336–2341

    Article  PubMed  CAS  Google Scholar 

  9. Institute of Medicine (2011) Dietary reference intakes for calcium and vitamin D. National Academies Press, Washington

    Google Scholar 

  10. Rizzoli R, Bonjour JP (2004) Dietary protein and bone health. J Bone Miner Res 19:527–531

    Article  PubMed  Google Scholar 

  11. Surdykowski AK, Kenny AM, Insogna KL, Kerstetter JE (2010) Optimizing bone health in older adults: the importance of dietary protein. Aging Health 6:345–357

    Article  PubMed  CAS  Google Scholar 

  12. Coin A, Sergi G, Benincá 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 

  13. 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  CAS  Google Scholar 

  14. Gaffney-Stomberg E, Insogna KL, Rodriguez NR, Kerstetter JE (2005) Increasing dietary protein requirements in elderly people for optimal muscle and bone health. J Am Geriatr Soc 5:1073–1079

    Google Scholar 

  15. Institute of Laboratory Animal Resources Commission on Life Sciences (ILARCLS) (1996) Guide for the care and use of laboratory animals. National Research Council, National Academies Press, Washington

    Google Scholar 

  16. Reeves PG, Nielsen FH, Fahey GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951

    PubMed  CAS  Google Scholar 

  17. Marotte C, Weisstaub A, Bryk G, Olguin MC, Posadas M, Lucero DM, Schreier L, Portela ML, Zeni SN (2013) Effect of dietary calcium (Ca) levels, on body weight, body composition, Ca absorption and retention during growth, in genetically obese (β) male rats. Eur J Nutr 52:297–305

    Article  PubMed  CAS  Google Scholar 

  18. Mastaglia S, Pellegrini G, Mandalunis P, Gonzales Chaves M, Friedman S, Zeni SN (2006) Vitamin D insufficiency reduces the protective effect of bisphosphonate on ovariectomy-induced bone loss in rats. Bone 39:837–844

    Article  PubMed  CAS  Google Scholar 

  19. Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:2–17

    Article  PubMed  Google Scholar 

  20. Hengsberger S, Ammann P, Legros B, Rizzoli R, Zysset P (2005) Intrinsic bone tissue properties in adult rat vertebrae: modulation by dietary protein. Bone 36:134–141

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  22. Albright F, Smith PH, Richardson AM (1941) Postmenopausal osteoporosis. J Am Med Assoc 116:2465–2474

    Article  Google Scholar 

  23. Bourrin S, Toromanoff A, 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 

  24. Dubois-Ferrière V, Brennan TC, Dayer R, Rizzoli R, Ammann P (2011) Calcitropic hormones and IGF-I are influenced by dietary protein. Endocrinology 152:1839–1847

    Article  PubMed  Google Scholar 

  25. Kerstetter JE, Looker AC, Insogna KL (2000) Low dietary protein and low bone density. Calcif Tissue Int 66:313

    Article  PubMed  CAS  Google Scholar 

  26. Kerstetter JE, O’Brien KO, Insogna KL (1998) Dietary protein affects intestinal calcium absorption. Am J Clin Nutr 68:859–865

    PubMed  CAS  Google Scholar 

  27. Kerstetter JE, Caseria DM, Mitnick ME, Ellison AF, Gay LF, Liskov TA, Carpenter TO, Insogna KL (1997) Increased circulating concentrations of parathyroid hormone in healthy, young women consuming a protein-restricted diet. Am J Clin Nutr 66:1188–1196

    PubMed  CAS  Google Scholar 

  28. Gomez JM (2006) The role of insulin-like growth factor I components in the regulation of vitamin D. Curr Pharm Biotechnol 7:125–132

    Article  PubMed  CAS  Google Scholar 

  29. Rosen CJ, Gallagher JC (2011) The 2011 IOM report on vitamin D and calcium requirements for North America: clinical implications for providers treating patients with low bone mineral density. J Clin Densitom 14:79–84

    Article  PubMed  Google Scholar 

  30. Ho KK, O’Sullivan AJ, Weissberger AJ, Kelly JJ (1996) Sex steroid regulation of growth hormone secretion and action. Horm Res 45:67–73

    Article  PubMed  CAS  Google Scholar 

  31. Chahal H, Drake W (2007) The endocrine system and aging. J Pathol 211:173–180

    Article  PubMed  CAS  Google Scholar 

  32. Ammann P, Bourrin S, Bonjour JP, Meyer JM, Rizzoli R (2000) Protein undernutrition-induced bone loss is associated with decreased IGF-I levels and estrogen deficiency. J Bone Miner Res 15:683–690

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the Buenos Aires University and the CONICET, and the OPD was provided in kind by Gador SA (Argentina). The authors acknowledge Julia Somoza for her technical assistance and Ricardo Orzuza from the General and Oral Biochemistry Department, School of Dentistry, Buenos Aires University, for his technical support and for taking care of the animals.

Conflict of interest

The authors report that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Metabolic Bone Diseases Laboratory, Clinical Hospital, Immunology, Genetic and Metabolism Institute (INIGEM), National Council for Scientific and Technologic Research (CONICET), Buenos Aires University, Buenos Aires, Argentina

    Clarisa Marotte, Macarena M. S. Gonzales Chaves, Gretel G. Pellegrini & Susana N. Zeni

  2. General and Oral Biochemistry Department, School of Dentistry, Buenos Aires University, Buenos Aires, Argentina

    Clarisa Marotte, Macarena M. S. Gonzales Chaves, Gretel G. Pellegrini, Silvia M. Friedman & Susana N. Zeni

  3. Pediatric Sunshine Academics and Sansum Diabetes Research Institute, Santa Barbara, CA, USA

    Clarisa Marotte, Fima Lifshitz & Susana N. Zeni

  4. Histology and Embryology Department, School of Dentistry, Buenos Aires University, Buenos Aires, Argentina

    Patricia Mandalunis

Authors
  1. Clarisa Marotte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Macarena M. S. Gonzales Chaves
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gretel G. Pellegrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvia M. Friedman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fima Lifshitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patricia Mandalunis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Susana N. Zeni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susana N. Zeni.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marotte, C., Gonzales Chaves, M.M.S., Pellegrini, G.G. et al. Low Protein Intake Magnifies Detrimental Effects of Ovariectomy and Vitamin D on Bone. Calcif Tissue Int 93, 184–192 (2013). https://doi.org/10.1007/s00223-013-9740-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-013-9740-8

Keywords

Search

Navigation