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Biological Trace Element Research

, Volume 156, Issue 1–3, pp 210–220 | Cite as

Preservation of Bone Structure and Function by Lithothamnion sp. Derived Minerals

  • Muhammad Nadeem Aslam
  • Ingrid Bergin
  • Karl Jepsen
  • Jaclynn M. Kreider
  • Kristin H. Graf
  • Madhav Naik
  • Steven A. Goldstein
  • James Varani
Article

Abstract

Progressive bone mineral loss and increasing bone fragility are hallmarks of osteoporosis. A combination of minerals isolated from the red marine algae, Lithothamnion sp. was examined for ability to inhibit bone mineral loss in female mice maintained on either a standard rodent chow (control) diet or a high-fat western diet (HFWD) for 5, 12, and 18 months. At each time point, femora were subjected to μ-CT analysis and biomechanical testing. A subset of caudal vertebrae was also analyzed. Following this, individual elements were assessed in bones. Serum levels of the 5b isoform of tartrate-resistant acid phosphatase (TRAP) and procollagen type I propeptide (P1NP) were also measured. Trabecular bone loss occurred in both diets (evident as early as 5 months). Cortical bone increased through month 5 and then declined. Cortical bone loss was primarily in mice on the HFWD. Inclusion of the minerals in the diet reduced bone mineral loss in both diets and improved bone strength. Bone mineral density was also enhanced by these minerals. Of several cationic minerals known to be important to bone health, only strontium was significantly increased in bone tissue from animals fed the mineral diets, but the increase was large (5–10 fold). Serum levels of TRAP were consistently higher in mice receiving the minerals, but levels of P1NP were not. These data suggest that trace minerals derived from marine red algae may be used to prevent progressive bone mineral loss in conjunction with calcium. Mineral supplementation could find use as part of an osteoporosis-prevention strategy.

Keywords

Bone Bone mineral density Bone mineral content Calcium Minerals Osteoporosis Red marine algae Strontium Trace elements 

Abbreviations

AIN76A

American Institute of Nutrition 76A

ANOVA

Analysis of variance

BMD

Bone mineral density

GRAS

Generally regarded as safe

HFWD

High-fat western-style diet

μ-CT

Microcomputed tomography

P1NP

N-terminal propeptide of type I procollagen

TRAP

Tartrate-resistant acid phosphatase (5b)

2D

Two-dimensional

3D

Three-dimensional

Notes

Acknowledgment

This study was supported in part by grant CA140760 from the National Institutes of Health, Bethesda, MD, and by grant 11-0577 from the Association for International Cancer Research, St. Andrews, Fife, Scotland. The authors would like to thank Marigot, Ltd. (Cork, Ireland) for providing the multi-mineral-rich supplement (Aquamin®) as a gift.

Disclosure of Conflict

All authors state that they have no financial or personal conflict of interest (no disclosures).

Supplementary material

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References

  1. 1.
    Prentice A (2004) Diet, nutrition and the prevention of osteoporosis. Public Health Nutr 7(1A):227–243PubMedCrossRefGoogle Scholar
  2. 2.
    De Laet CE, Van Hout BA, Burger H, Weel AE, Hofman A, Pols HA (1998) Hip fracture prediction in elderly men and women: validation in the Rotterdam study. J Bone Miner Res 13:1587–1593PubMedCrossRefGoogle Scholar
  3. 3.
    Iskrant AP (1968) The etiology of fractured hips in females. Am J Public Health 58:485–490CrossRefGoogle Scholar
  4. 4.
    Prentice A (1997) Is nutrition important in osteoporosis? Proc Nutr Soc 56:357–367PubMedCrossRefGoogle Scholar
  5. 5.
    Rosen CJ, Klibanski A (2009) Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med 122:409–414PubMedCrossRefGoogle Scholar
  6. 6.
    Kato I, Toniolo P, Zeleniuch-Jacquotte A, Shore RE, Koenig KL, Akhmedkhanov A, Riboli E (2000) Diet, smoking and anthropometric indices and postmenopausal bone fractures: a prospective study. Int J Epidemiol 29:85–92PubMedCrossRefGoogle Scholar
  7. 7.
    Zernicke RF, Salem GJ, Barnard RJ, Schramm E (1995) Long-term high-fat sucrose diet alters rat femoral neck and vertebral morphology, bone mineral content and mechanical properties. Bone 16:25–31PubMedGoogle Scholar
  8. 8.
    Ionova-Martin SS, Do SH, Barth HD, Szadkowska M, Porter AE, Ager JW 3rd, Ager JW Jr, Alliston T, Vaisse C, Ritchie RO (2010) Reduced size-independent mechanical properties of cortical bone in high-fat diet-induced obesity. Bone 46(1):217–225PubMedCrossRefGoogle Scholar
  9. 9.
    Glatt V, Canalis E, Stadmeyer L, Bouxsein ML (2007) Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J Bone Mineral Res 22:1197–1207CrossRefGoogle Scholar
  10. 10.
    Heaney RP, Weaver CM (2005) Newer perspectives on calcium nutrition and bone quality. J Am Coll Nutr 24:574S–581SPubMedCrossRefGoogle Scholar
  11. 11.
    Peacock M, Liu G, Carey M, McClintock R, Ambrosius W, Hui S, Johnston CC (2000) Effect of a calcium or 25OHD vitamin D3 dietary supplementation on bone loss at the hip in men and women over the age of 60. J Clin Endocrinol Metab 85(9):3011–3019PubMedCrossRefGoogle Scholar
  12. 12.
    Royal College of Physicians (1999) Osteoporosis: clinical guidelines for prevention and treatment. Royal College of Physicians, LondonGoogle Scholar
  13. 13.
    Odabasi E, Turan M, Aydin A, Akay C, Kutlu M (2008) Magnesium, zinc, copper, manganese and selenium levels in postmenopausal women with osteoporosis: can magnesium play a key role in osteoporosis? Ann Acad Med Singapore 37(7):564–567PubMedGoogle Scholar
  14. 14.
    Lowe NM, Lowe NM, Fraser WD, Jackson MJ (2002) Is there potential therapeutic value of copper and zinc for osteoporosis? Proc Nutr Soc 61(2):181–185PubMedCrossRefGoogle Scholar
  15. 15.
    Stause L, Saltman P, Smith KT, Bracker M, Andon MB (1994) Spinal bone loss in post-menopausal women supplemented with calcium and trace metals. J Nutr 124(7):1060–1064Google Scholar
  16. 16.
    Jugdaohsingh R (2007) Silicon and bone health. J Nutr Health Aging 11(2):99–110PubMedGoogle Scholar
  17. 17.
    Marie PJ, Ammann P, Boivin G, Rey C (2001) Mechanisms of action and therapeutic potential of strontium in bone. Calc Tissue Int 69(3):121–129CrossRefGoogle Scholar
  18. 18.
    Cashman K, Flynn A (1998) Trace elements and bone metabolism. In: Sandstrom B, Walter P (eds) Role of trace elements for health promotion and disease prevention. Bibl Nutr Dieta. Karger, Basel, vol 54, pp. 150–164Google Scholar
  19. 19.
    Yamaguchi M (1998) Role of zinc in bone formation and bone resorption. J Trace Elem Exp Med 11:119–135CrossRefGoogle Scholar
  20. 20.
    Adluri RS, Zhan L, Bagchi M, Maulik N, Maulik G (2010) Comparative effects of a novel plant-based calcium supplement with two common calcium salts on proliferation and mineralization in human osteoblast cells. Mol Cell Biochem 340(1–2):73–80PubMedCrossRefGoogle Scholar
  21. 21.
    Aslam MN, Paruchuri T, Bhagavathula N, Varani J (2010) A mineral- rich red algae extract inhibits polyp formation and inflammation in the gastrointestinal tract of mice on a high-fat diet. Integr Cancer Ther 9(1):93–99PubMedCrossRefGoogle Scholar
  22. 22.
    Aslam MN, Bergin I, Naik M, Paruchuri T, Hampton A, Rehman M, Dame MK, Rush H, Varani J (2012) A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice. Nutr Cancer 64(7):1020–1028PubMedCrossRefGoogle Scholar
  23. 23.
    Aslam MN, Bergin I, Naik M, Hampton A, Allen R, Kunkel SL, Rush H, Varani J (2012) A multi-mineral natural product inhibits liver tumor formation in C57BL/6 mice. Biol Trace Elem Res 147(1–3):267–274PubMedCrossRefGoogle Scholar
  24. 24.
    Aslam MN, Kreider JM, Paruchuri T, Bhagavathula N, DaSilva M, Zernicke RF, Goldstein SA, Varani J (2010) A mineral-rich extract from the red marine algae lithothamnion calcareum preserves bone structure and function in female mice on a Western-style diet. Calcif Tissue Int 86(4):313–324PubMedCrossRefGoogle Scholar
  25. 25.
    Newmark HL, Yang K, Lipkin M, Kopelovich L, Liu Y, Fan K, Shinozaki H (2001) A Western-style diet induces benign and malignant neoplasms in the colon of normal C57BL/6 mice. Carcinogenesis 22(11):1871–1875PubMedCrossRefGoogle Scholar
  26. 26.
    Lipkin M, Reddy B, Newmark H, Lamprecht SA (1999) Dietary factors in human colorectal cancer. Annu Rev Nutr 19:545–586PubMedCrossRefGoogle Scholar
  27. 27.
    Meganck JA, Kozloff KM, Thornton MM, Broski SM, Goldstein SA (2009) Beam hardening artifacts in micro-computed tomography scanning can be reduced by X-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone 45(6):1104–1106PubMedCrossRefGoogle Scholar
  28. 28.
    Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25(7):1468–1486PubMedCrossRefGoogle Scholar
  29. 29.
    Salem GJ, Zernicke RF, Martinez DA, Vailas AC (1993) Adaptations of immature trabecular bone to moderate exercise: geometrical, biochemical, and biomechanical correlates. Bone 14(4):647–654PubMedCrossRefGoogle Scholar
  30. 30.
    Tommasini SM, Wearne SL, Hof PR, Jepsen KJ (2008) Percolation theory relates corticocancellaous architecture to mechanical function in vertebrae of inbred mouse strains. Bone 42(4):743–750PubMedCrossRefGoogle Scholar
  31. 31.
    Hannon RA, Clowes JA, Eagleton AC, Al Hadari AA, Eastell R, Blumsohn A (2004) Clinical performance of immunoreactive tartrate resistant acid phosphatase isoform 5b as a marker of bone resorption. Bone 34(1):187–194PubMedCrossRefGoogle Scholar
  32. 32.
    Alatalo SL, Halleen JM, Hentunen TA, Monkkonen J, Vaananen JH (2000) Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium. Clin Chem 46(11):1751–1754PubMedGoogle Scholar
  33. 33.
    Risteli J, Risteli L (2006) Products of bone collagen metabolism. In: Seibel MJ, Robins SP, Bilezikian JP, Seibel MJ, Robins SP, Bilezikian JP G (eds) Dynamics of bone and cartilage metabolism: principles and clinical applications, 2nd edn. Academic, London, pp 391–405CrossRefGoogle Scholar
  34. 34.
    Peterlik H, Roschger P, Klauhofer K, Fratzl P (2006) From brittle to ductile fracture of bone. Nat Mater 5(1):52–55PubMedCrossRefGoogle Scholar
  35. 35.
    Loro ML, Sayre J, Roe TF, Goran MI, Kaufman FR, Gilsanz V (2000) Early identification of children predisposed to low peak bone mass and osteoporosis later in life. J Clin Endocrinol Metab 85(10):3908–3918PubMedCrossRefGoogle Scholar
  36. 36.
    Khosla S (2003) Surrogates for fracture endpoints in clinical trials. J Bone Miner Res 18(6):1146–1149PubMedCrossRefGoogle Scholar
  37. 37.
    Roberts NB, Wassh HPJ, Klenerman L, Kelly SA, Helliwell TR (1996) Determination of elements in human femoral bone using inductively coupled plasma atomic emission spectrmetry and inductively coupled plasma mass spectrometry. J Anal At Spectrom 11:133–138CrossRefGoogle Scholar
  38. 38.
    Zhang YX, Wang YS, Zhang YP, Zhang GL, Huang YY, He W (2007) Investigation of elemental distribution in human femoral head by PIXE and SRXRF microprobe. Nucl Instrum Methods Phys Res 260:178–183CrossRefGoogle Scholar
  39. 39.
    Saidak Z, Marie PJ (2012) Strontium signaling: molecular mechanisms and therapeutic implications in osteoporosis. Pharmacol Ther 136(2):216–226PubMedCrossRefGoogle Scholar
  40. 40.
    Meunier PJ, Roux C, Seeman E, Ortolani S, Badurski JE, Spector TD, Cannata J, Balogh A, Lemmel EM, Pors-Nielsen S, Rizzoli R, Genant HK, Reginster JY (2004) The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. N Engl J Med 350(5):459–468PubMedCrossRefGoogle Scholar
  41. 41.
    Ammann P, Shen V, Robin B, Mauras Y, Bonjour JP, Rizzoli R (2004) Strontium ranelate improves bone resistance by increasing bone mass and improving architecture in intact female rats. J Bone Miner Res 19(12):2012–2020PubMedCrossRefGoogle Scholar
  42. 42.
    LeGeros RZ (1990) Chemical and crystallographic events in the caries process. J Dent Res 69:567–574, discussion 634–6PubMedGoogle Scholar
  43. 43.
    Thornton JR (1981) High colonic pH promotes colorectal cancer. Lancet 1(8229):1081–1083PubMedCrossRefGoogle Scholar
  44. 44.
    Cashman KD (2008) Altered bone metabolism in inflammatory disease: role for nutrition. Proc Nutr Soc 67(2):196–205PubMedCrossRefGoogle Scholar
  45. 45.
    Frestedt JL, Walsh M, Kuskowski MA, Zenk JL (2008) A natural mineral supplement provides relief from knee osteoarthritis symptoms: a randomized controlled pilot trial. Nutr J 7:9PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Muhammad Nadeem Aslam
    • 1
  • Ingrid Bergin
    • 2
  • Karl Jepsen
    • 3
  • Jaclynn M. Kreider
    • 3
  • Kristin H. Graf
    • 3
  • Madhav Naik
    • 1
  • Steven A. Goldstein
    • 3
  • James Varani
    • 1
  1. 1.Department of PathologyThe University of MichiganAnn ArborUSA
  2. 2.The Unit for Laboratory Animal MedicineThe University of MichiganAnn ArborUSA
  3. 3.Department of Orthopaedic SurgeryThe University of MichiganAnn ArborUSA

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