Interactions of Dietary Patterns, Systemic Inflammation, and Bone Health

Chapter

Abstract

Examination of combinations of foods, as described by dietary patterns in relation to health indices, may be an important approach to further our understanding of chronic disease prevention. Bone loss is a common factor in many chronic inflammatory conditions, although it is unclear whether low-grade systemic inflammation may have similar long-term effects. In this chapter we summarize current evidence relating dietary patterns and chronic low-grade systemic inflammation to bone health. Consideration is then given to potential mechanisms whereby dietary eating patterns may affect inflammatory status. Dietary patterns rich in fruits and vegetables consistently appear to have a protective effect on bone mineral density, likely due to their abundance of micronutrients, minerals, and bioactive compounds. Current evidence relating low-grade systemic inflammation to indices of bone health is limited and contradictory, although modification of dietary eating habits (increasing intakes of plant-based foods and reducing the omega-6 to omega-3 fatty acid ratio) may be important in the management of chronic inflammatory status. Longitudinal studies assessing dietary patterns in relation to bone mineral density/fracture incidence and biomarkers of inflammation could further our understanding of these complex interactions.

Keywords

Dietary patterns Systemic inflammation Bone mineral density Fracture Chronic disease prevention 

References

  1. 1.
    Wharton B, Bishop N. Rickets. Lancet. 2002;362:1389–400.CrossRefGoogle Scholar
  2. 2.
    Bischoff-Ferrari HA, Willett WC, Orav EJ, Lips P, Meunier PJ, et al. A pooled analysis of vitamin D dose requirements for fracture prevention. N Engl J Med. 2012;367:40–9.PubMedCrossRefGoogle Scholar
  3. 3.
    New SA, Robins SP, Campbell MK, Martin JC, Garton MJ, et al. Dietary influences on bone mass and bone metabolism: further evidence of a positive link between fruit and vegetable consumption and bone health? Am J Clin Nutr. 2000;71:142–51.PubMedGoogle Scholar
  4. 4.
    Macdonald HM, New SA, Golden MH, Campbell MK, Reid DM. Nutritional associations with bone loss during the menopausal transition: evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids. Am J Clin Nutr. 2004;79:155–65.PubMedGoogle Scholar
  5. 5.
    Macdonald HM, Black AJ, Aucott L, Duthie G, Duthie S, et al. Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: a randomized controlled trial. Am J Clin Nutr. 2008;88:465–74.PubMedGoogle Scholar
  6. 6.
    Cockayne S, Adamson J, Lanham-New S, Shearer MJ, Gilbody S, et al. Vitamin K and the prevention of fractures: systematic review and meta-analysis of randomized controlled trials. Arch Intern Med. 2006;166:1256–61.PubMedCrossRefGoogle Scholar
  7. 7.
    Hegarty VM, May HM, Khaw KT. Tea drinking and bone mineral density in older women. Am J Clin Nutr. 2000;71:1003–7.PubMedGoogle Scholar
  8. 8.
    Tucker KL, Morita K, Qiao N, Hannan MT, Cupples LA, et al. Colas, but not other carbonated beverages, are associated with low bone mineral density in older women: the Framingham Osteoporosis Study. Am J Clin Nutr. 2006;84:936–42.PubMedGoogle Scholar
  9. 9.
    Hannan MT, Tucker KL, Dawson-Hughes B, Cupples LA, Felson DT, et al. Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res. 2000;15:2504–12.PubMedCrossRefGoogle Scholar
  10. 10.
    Jacobs Jr DR, Steffen LM. Nutrients, foods, and dietary patterns as exposures in research: a framework for food synergy. Am J Clin Nutr. 2003;78:508S–13.PubMedGoogle Scholar
  11. 11.
    Hu FB. Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol. 2002;13:3–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Jacques PF, Tucker KL. Are dietary patterns useful for understanding the role of diet in chronic disease? Am J Clin Nutr. 2001;73:1–2.PubMedGoogle Scholar
  13. 13.
    Kant AK. Dietary patterns and health outcomes. J Am Diet Assoc. 2004;104:615–35.PubMedCrossRefGoogle Scholar
  14. 14.
    Macdonald HM, Hardcastle AC. Dietary patterns and bone health. In: Burckhardt P, Dawsonhughes B, Weaver C, editors. Nutritional influences on bone health. London: Springer; 2002.Google Scholar
  15. 15.
    Newby PK, Tucker KL. Empirically derived eating patterns using factor or cluster analysis: a review. Nutr Rev. 2004;62:177–203.PubMedCrossRefGoogle Scholar
  16. 16.
    Hardy R, Cooper MS. Bone loss in inflammatory disorders. J Endocrinol. 2009;201:309–20.PubMedCrossRefGoogle Scholar
  17. 17.
    Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, et al. Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr. 2002;76:245–52.PubMedGoogle Scholar
  18. 18.
    Okubo H, Sasaki S, Horiguchi H, Oguma E, Miyamoto K, et al. Dietary patterns associated with bone mineral density in premenopausal Japanese farmwomen. Am J Clin Nutr. 2006;83:1185–92.PubMedGoogle Scholar
  19. 19.
    Kontogianni MD, Melistas L, Yannakoulia M, Malagaris I, Panagiotakos DB, et al. Association between dietary patterns and indices of bone mass in a sample of Mediterranean women. Nutrition. 2009;25:165–71.PubMedCrossRefGoogle Scholar
  20. 20.
    Langsetmo L, Poliquin S, Hanley DA, Prior JC, Barr S, et al. Dietary patterns in Canadian men and women ages 25 and older: relationship to demographics, body mass index, and bone mineral density. BMC Musculoskelet Disord. 2010;11:20.PubMedCrossRefGoogle Scholar
  21. 21.
    Hardcastle AC, Aucott L, Fraser WD, Reid DM, Macdonald HM. Dietary patterns, bone resorption and bone mineral density in early post-menopausal Scottish women. Eur J Clin Nutr. 2011;65:378–85.PubMedCrossRefGoogle Scholar
  22. 22.
    Langsetmo L, Hanley DA, Prior JC, Barr SI, Anastassiades T, et al. Dietary patterns and incident low-trauma fractures in postmenopausal women and men aged >/= 50 y: a population-based cohort study. Am J Clin Nutr. 2011;93:192–9.PubMedCrossRefGoogle Scholar
  23. 23.
    McNaughton SA, Wattanapenpaiboon N, Wark JD, Nowson CA. An energy-dense, nutrient-poor dietary pattern is inversely associated with bone health in women. J Nutr. 2011;141:1516–23.PubMedCrossRefGoogle Scholar
  24. 24.
    Karamati M, Jessri M, Shariati-Bafghi SE, Rashidkhani B. Dietary patterns in relation to bone mineral density among menopausal Iranian women. Calcif Tissue Int. 2012;91:40–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Whittle CR, Woodside JV, Cardwell CR, McCourt HJ, Young IS, et al. Dietary patterns and bone mineral status in young adults: the Northern Ireland Young Hearts Project. Br J Nutr. 2012;108:1494–504.PubMedCrossRefGoogle Scholar
  26. 26.
    Wachman A, Bernstein DS. Diet and osteoporosis. Lancet. 1968;1:958–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Macdonald H. Influence of organic salts of potassium on bone health: possible mechanisms of action for the role of fruit and vegetables. In: Burckhardt P, Weaver C, Dawsonhughes B, editors. Nutritional aspects of osteoporosis. London: Elsevier/Academic Press; 2007. p. 268–81.Google Scholar
  28. 28.
    Jesudason D, Clifton P. The interaction between dietary protein and bone health. J Bone Miner Metab. 2011;29:1–14.PubMedCrossRefGoogle Scholar
  29. 29.
    Gough AK, Lilley J, Eyre S, Holder RL, Emery P. Generalised bone loss in patients with early rheumatoid arthritis. Lancet. 1994;344:23–7.PubMedCrossRefGoogle Scholar
  30. 30.
    Spector TD, Hall GM, McCloskey EV, Kanis JA. Risk of vertebral fracture in women with rheumatoid arthritis. BMJ. 1993;306:558.PubMedCrossRefGoogle Scholar
  31. 31.
    Bernstein CN, Blanchard JF, Leslie W, Wajda A, Yu BN. The incidence of fracture among patients with inflammatory bowel disease. A population-based cohort study. Ann Intern Med. 2000;133:795–9.PubMedGoogle Scholar
  32. 32.
    Loftus Jr EV, Crowson CS, Sandborn WJ, Tremaine WJ, O’Fallon WM, et al. Long-term fracture risk in patients with Crohn’s disease: a population-­based study in Olmsted County, Minnesota. Gastroenterology. 2002;123:468–75.PubMedCrossRefGoogle Scholar
  33. 33.
    Lane NE. Therapy insight: osteoporosis and osteonecrosis in systemic lupus erythematosus. Nat Clin Pract Rheumatol. 2006;2:562–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Geusens P, Vosse D, van der Linden S. Osteoporosis and vertebral fractures in ankylosing spondylitis. Curr Opin Rheumatol. 2007;19:335–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Barnes PJ, Celli BR. Systemic manifestations and comorbidities of COPD. Eur Respir J. 2009;33:1165–85.PubMedCrossRefGoogle Scholar
  36. 36.
    Lorenzo J, Horowitz M, Choi Y. Osteoimmunology: interactions of the bone and immune system. Endocr Rev. 2008;29:403–40.PubMedCrossRefGoogle Scholar
  37. 37.
    Du Clos TW. Function of C-reactive protein. Ann Med. 2000;32:274–8.PubMedCrossRefGoogle Scholar
  38. 38.
    Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342:836–43.PubMedCrossRefGoogle Scholar
  39. 39.
    Pai JK, Pischon T, Ma J, Manson JE, Hankinson SE, et al. Inflammatory markers and the risk of coronary heart disease in men and women. N Engl J Med. 2004;351:2599–610.PubMedCrossRefGoogle Scholar
  40. 40.
    Mosca L, Benjamin EJ, Berra K, Bezanson JL, Dolor RJ, et al. Effectiveness-based guidelines for the prevention of cardiovascular disease in women – 2011 update: a guideline from the American Heart Association. Circulation. 2011;123:1243–62.PubMedCrossRefGoogle Scholar
  41. 41.
    Koh JM, Khang YH, Jung CH, Bae S, Kim DJ, et al. Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: evidence for a link between systemic inflammation and osteoporosis. Osteoporos Int. 2005;16:1263–71.PubMedCrossRefGoogle Scholar
  42. 42.
    Ganesan K, Teklehaimanot S, Tran TH, Asuncion M, Norris K. Relationship of C-reactive protein and bone mineral density in community-dwelling elderly females. J Natl Med Assoc. 2005;97:329–33.PubMedGoogle Scholar
  43. 43.
    Pasco JA, Kotowicz MA, Henry MJ, Nicholson GC, Spilsbury HJ, et al. High-sensitivity C-reactive protein and fracture risk in elderly women. JAMA. 2006;296:1353–5.PubMedCrossRefGoogle Scholar
  44. 44.
    Schett G, Kiechl S, Weger S, Pederiva A, Mayr A, et al. High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch Intern Med. 2006;166:2495–501.PubMedCrossRefGoogle Scholar
  45. 45.
    Bhupathiraju SN, Alekel DL, Stewart JW, Hanson LN, Shedd KM, et al. Relationship of circulating total homocysteine and C-reactive protein to trabecular bone in postmenopausal women. J Clin Densitom. 2007;10:395–403.PubMedCrossRefGoogle Scholar
  46. 46.
    Ding C, Parameswaran V, Udayan R, Burgess J, Jones G. Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab. 2008;93:1952–8.PubMedCrossRefGoogle Scholar
  47. 47.
    de Pablo P, Cooper MS, Buckley CD. Association between bone mineral density and C-reactive protein in a large population-based sample. Arthritis Rheum. 2012;64(8):2624–31.PubMedCrossRefGoogle Scholar
  48. 48.
    Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, et al. Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res. 2007;22:1088–95.PubMedCrossRefGoogle Scholar
  49. 49.
    Haddad PS, Azar GA, Groom S, Boivin M. Natural health products, modulation of immune function and prevention of chronic diseases. Evid Based Com­plement Alternat Med. 2005;2:513–20.PubMedCrossRefGoogle Scholar
  50. 50.
    Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr. 2005;81:341–54.PubMedGoogle Scholar
  51. 51.
    Lopez-Garcia E, Schulze MB, Meigs JB, Manson JE, Rifai N, et al. Consumption of trans fatty acids is related to plasma biomarkers of inflammation and endothelial dysfunction. J Nutr. 2005;135:562–6.PubMedGoogle Scholar
  52. 52.
    Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, et al. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem. 1994;269:9889–97.PubMedGoogle Scholar
  53. 53.
    Liu RH. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr. 2003;78:517S–20.PubMedGoogle Scholar
  54. 54.
    Acamovic T, Brooker JD. Biochemistry of plant secondary metabolites and their effects in animals. Proc Nutr Soc. 2005;64:403–12.PubMedCrossRefGoogle Scholar
  55. 55.
    Guo W, Kong E, Meydani M. Dietary polyphenols, inflammation, and cancer. Nutr Cancer. 2009;61:807–10.PubMedCrossRefGoogle Scholar
  56. 56.
    Garcia-Lafuente A, Guillamon E, Villares A, Rostagno MA, Martinez JA. Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflamm Res. 2009;58:537–52.PubMedCrossRefGoogle Scholar
  57. 57.
    Kim HP, Son KH, Chang HW, Kang SS. Anti-inflammatory plant flavonoids and cellular action mechanisms. J Pharmacol Sci. 2004;96:229–45.PubMedCrossRefGoogle Scholar
  58. 58.
    Lee YH, Choi SJ, Ji JD, Song GG. Associations between ERAP1 polymorphisms and ankylosing spondylitis susceptibility: a meta-analysis. Inflamm Res. 2011;60:999–1003.PubMedCrossRefGoogle Scholar
  59. 59.
    Park HJ, Jeong SK, Kim SR, Bae SK, Kim WS, et al. Resveratrol inhibits Porphyromonas gingivalis lipo­polysaccharide-induced endothelial adhesion molecule expression by suppressing NF-kappaB activation. Arch Pharm Res. 2009;32:583–91.PubMedCrossRefGoogle Scholar
  60. 60.
    Rahman I, Biswas SK, Kirkham PA. Regulation of inflammation and redox signaling by dietary polyphenols. Biochem Pharmacol. 2006;72:1439–52.PubMedCrossRefGoogle Scholar
  61. 61.
    Gloire G, Legrand-Poels S, Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol. 2006;72:1493–505.PubMedCrossRefGoogle Scholar
  62. 62.
    Visioli F, Poli A, Richard D, Paoletti R. Modulation of inflammation by nutritional interventions. Curr Atheroscler Rep. 2008;10:451–3.PubMedCrossRefGoogle Scholar
  63. 63.
    Pischon T, Hankinson SE, Hotamisligil GS, Rifai N, Willett WC, et al. Habitual dietary intake of n-3 and n-6 fatty acids in relation to inflammatory markers among US men and women. Circulation. 2003;108:155–60.PubMedCrossRefGoogle Scholar
  64. 64.
    Russo GL. Dietary n-6 and n-3 polyunsaturated fatty acids: from biochemistry to clinical implications in cardiovascular prevention. Biochem Pharmacol. 2009;77:937–46.PubMedCrossRefGoogle Scholar
  65. 65.
    North CJ, Venter CS, Jerling JC. The effects of dietary fibre on C-reactive protein, an inflammation marker predicting cardiovascular disease. Eur J Clin Nutr. 2009;63:921–33.PubMedCrossRefGoogle Scholar
  66. 66.
    Galland L. Diet and inflammation. Nutr Clin Pract. 2010;25:634–40.PubMedCrossRefGoogle Scholar
  67. 67.
    Barr R, Macdonald H, Stewart A, McGuigan F, Rogers A, et al. Association between vitamin D receptor gene polymorphisms, falls, balance and muscle power: results from two independent studies (APOSS and OPUS). Osteoporos Int. 2010;21:457–66.PubMedCrossRefGoogle Scholar
  68. 68.
    Masson LF, McNeill G, Tomany JO, Simpson JA, Peace HS, et al. Statistical approaches for assessing the relative validity of a food-frequency questionnaire: use of correlation coefficients and the kappa statistic. Public Health Nutr. 2003;6:313–21.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2013

Authors and Affiliations

  1. 1.Department of Musculoskeletal ResearchUniversity of AberdeenAberdeenUK

Personalised recommendations