The association of red blood cell n-3 and n-6 fatty acids with bone mineral density and hip fracture risk in the women's health initiative

Journal of Bone and Mineral Research

Volumn 28, Issue 3, 2013, Pages 505-515

  Orchard, Tonya S ^a   Ing, Steven W ^b   Lu, Bo ^a   Belury, Martha A ^a   Johnson, Karen ^c   Wactawski Wende, Jean ^d,e   Jackson, Rebecca D ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

^e UNIVERSITY AT BUFFALO   (United States)

Author keywords

BONE MINERAL DENSITY; HIP FRACTURE; OMEGA 3 (N 3) FATTY ACIDS; OMEGA 6 (N 6) FATTY ACIDS; POLYUNSATURATED FATTY ACIDS

Indexed keywords

ARACHIDONIC ACID; CALCIUM; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; LINOLEIC ACID; LINOLENIC ACID; MONOUNSATURATED FATTY ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; SATURATED FATTY ACID;

AGED; ARTICLE; BONE DENSITY; CALCIUM INTAKE; CALORIC INTAKE; CONTROLLED STUDY; DIETARY INTAKE; ERYTHROCYTE; FEMALE; FOLLOW UP; GAS CHROMATOGRAPHY; HIP; HIP FRACTURE; HUMAN; LUMBAR SPINE; MAJOR CLINICAL STUDY; POSTMENOPAUSE; PROSPECTIVE STUDY; RACE; RISK ASSESSMENT;

AGED; BONE DENSITY; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FEMALE; HUMANS; PROSPECTIVE STUDIES; WOMEN'S HEALTH;

EID: 84873963399     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1772     Document Type: Article

References (63)

1. Braithwaite RS, Col NF, Wong JB., Estimating hip fracture morbidity, mortality and costs. J Am Geriatr Soc. 2003; 51 (3): 364-70.
2. Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A., Incidence and economic burden of osteoporosis-related fractures in the United States. 2005-2025. J Bone Miner Res. 2007; 22 (3): 465-75.
3. Calder PC., Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie. 2009; 91 (6): 791-5.
4. Poulsen RC, Gotlinger KH, Serhan CN, Kruger MC., Identification of inflammatory and proresolving lipid mediators in bone marrow and their lipidomic profiles with ovariectomy and omega-3 intake. Am J Hematol. 2008; 83 (6): 437-45.
5. Hofbauer LC, Schoppet M., Clinical implications, of the, osteoprotegerin/RANKL/RANK system, for bone, vascular diseases. JAMA. 2004; 292 (4): 490-5. DOI: 10.1001/jama.292.4.490
6. Watkins BA, Li Y, Seifert MF., Nutraceutical fatty acids as biochemical and molecular modulators of skeletal biology. J Am Coll Nutr. 2001; 20 (5 Suppl):410S-6S; discussion 417S-20S.
7. Coetzee M, Haag M, Kruger MC., Effects of arachidonic acid, docosahexaenoic acid, prostaglandin E(2) and parathyroid hormone on osteoprotegerin and RANKL secretion by MC3T3-E1 osteoblast-like cells. J Nutr Biochem. 2007; 18 (1): 54-63.
8. Zwart SR, Pierson D, Mehta S, Gonda S, Smith SM., Capacity of omega-3 fatty acids or eicosapentaenoic acid to counteract weightlessness-induced bone loss by inhibiting NF-kappaB activation: from cells to bed rest to astronauts. J Bone Miner Res. 2010; 25 (5): 1049-57. DOI: 10.1359/jbmr.091041
9. Sun L, Tamaki H, Ishimaru T, Teruya T, Ohta Y, Katsuyama N, Chinen I., Inhibition of osteoporosis due to restricted food intake by the fish oils DHA and EPA and perilla oil in the rat. Biosci Biotechnol Biochem. 2004; 68 (12): 2613-5.
10. Baggio B, Budakovic A, Nassuato MA, Vezzoli G, Manzato E, Luisetto G, Zaninotto M., Plasma phospholipid arachidonic acid content and calcium metabolism in idiopathic calcium nephrolithiasis. Kidney Int. 2000; 58 (3): 1278-84.
11. Haag M, Magada ON, Claassen N, Bohmer LH, Kruger MC., Omega-3 fatty acids modulate ATPases involved in duodenal Ca absorption. Prostaglandins Leukot Essent Fatty Acids. 2003; 68 (6): 423-9.
12. Haag M, Kruger MC., Upregulation of duodenal calcium absorption by poly-unsaturated fatty acids: events at the basolateral membrane. Med Hypotheses. 2001; 56 (5): 637-40.
13. Huang JT, Welch JS, Ricote M, Binder CJ, Willson TM, Kelly C, Witztum JL, Funk CD, Conrad D, Glass CK., Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature. 1999; 400 (6742): 378-82.
14. Duque G., As a matter of fat: new perspectives on the understanding of age-related bone loss. Bonekey Osteovision. 2007; 4 (4): 129-40.
15. Deckelbaum RJ, Worgall TS, Seo T., n-3 Fatty acids and gene expression. Am J Clin Nutr. 2006; 83 (6): S1520-5.
16. Shen CL, Yeh JK, Rasty J, Li Y, Watkins BA., Protective effect of dietary long-chain n-3 polyunsaturated fatty acids on bone loss in gonad-intact middle-aged male rats. Br J Nutr. 2006; 95 (3): 462-8.
17. Watkins BA, Li Y, Seifert MF., Dietary ratio of n-6/n-3 PUFAs and docosahexaenoic acid: actions on bone mineral and serum biomarkers in ovariectomized rats. J Nutr Biochem. 2006; 17 (4): 282-9.
18. Suzuki T, Yoshida H, Hashimoto T, Yoshimura N, Fujiwara S, Fukunaga M, Nakamura T, Yoh K, Inoue T, Hosoi T, Orimo H., Case-control study of risk factors for hip fractures in the Japanese elderly by a Mediterranean Osteoporosis Study (MEDOS) questionnaire. Bone. 1997; 21 (5): 461-7. Cited. in: PubMed; PMID. 9356741.
19. Appleby P, Roddam A, Allen N, Key T., Comparative fracture risk in vegetarians and nonvegetarians in EPIC-Oxford. Eur J Clin Nutr. 2007; 61 (12): 1400-6.
20. Virtanen JK, Mozaffarian D, Cauley JA, Mukamal KJ, Robbins J, Siscovick DS., Fish consumption, bone mineral density, and risk of hip fracture among older adults: the cardiovascular health study. J Bone Miner Res. 2010; 25 (9): 1972-9.
21. Farina EK, Kiel DP, Roubenoff R, Schaefer EJ, Cupples LA, Tucker KL., Dietary Intakes of arachidonic acid and {alpha}-linolenic acid are associated with reduced risk of hip fracture in older adults. J Nutr. 2011; 141 (6): 1146-53.
22. Orchard TS, Cauley JA, Frank GC, Neuhouser ML, Robinson JG, Snetselaar L, Tylavsky F, Wactawski-Wende J, Young AM, Lu B, Jackson RD., Fatty acid consumption and risk of fracture in the Women's Health Initiative. Am J Clin Nutr. 2010 Dec; 92 (6): 1452-60.
23. Hogstrom M, Nordstrom P, Nordstrom A., n-3 Fatty acids are positively associated with peak bone mineral density and bone accrual in healthy men: the NO2 Study. Am J Clin Nutr. 2007; 85 (3): 803-7.
24. Harris WS., Omega-3 fatty acids and cardiovascular disease: A case for omega-3 index as a new risk factor. Pharmacol Res. 2007; 55 (3): 217-23.
25. Truong H, DiBello JR, Ruiz-Narvaez E, Kraft P, Campos H, Baylin A., Does genetic variation in the Delta6-desaturase promoter modify the association between alpha-linolenic acid and the prevalence of metabolic syndrome?. Am J Clin Nutr. 2009; 89 (3): 920-5.
26. Block RC, Harris WS, Reid KJ, Sands SA, Spertus JA., EPA and DHA in blood cell membranes from acute coronary syndrome patients and controls. Atherosclerosis. 2008; 197 (2): 821-8.
27. Sun Q, Ma J, Campos H, Hankinson SE., Hu FB., Comparison between plasma and erythrocyte fatty acid content as biomarkers of fatty acid intake in US women. Am J Clin Nutr. 2007; 86 (1): 74-81.
28. Harris WS, Pottala JV, Sands SA, Jones PG., Comparison of the effects of fish and fish-oil capsules on the n 3 fatty acid content of blood cells and plasma phospholipids. Am J Clin Nutr. 2007; 86 (6): 1621-5.
29. Harris WS, Thomas RM., Biological variability of blood omega-3 biomarkers. Clin Biochem. 2009; 43 (3): 338-40.
30. Godley PA, Campbell MK, Miller C, Gallagher P, Martinson FE, Mohler JL, et al. Correlation between biomarkers of omega-3 fatty acid consumption and questionnaire data in African American and Caucasian United States males with and without prostatic carcinoma. Cancer Epidemiol Biomarkers Prev. 1996; 5 (2): 115-9.
31. Design of the Women's Health Initiative clinical trial and observational study. The Women's Health Initiative Study Group. Control Clin Trials. 1998; 19 (1): 61-109. Cited. in: PubMed; PMID. 9492970.
32. LaCroix AZ, Beck TJ, Cauley JA, Lewis CE, Bassford T, Jackson R, Wu G, Chen Z., Hip structural geometry and incidence of hip fracture in postmenopausal women: what does it add to conventional bone mineral density?. Osteoporos Int. 2010; 21 (6): 919-29.
33. Curb JD, McTiernan A, Heckbert SR, Kooperberg C, Stanford J, Nevitt M, Johnson KC, Proulx-Burns L, Pastore L, Criqui M., Daugherty S; WHI Morbidity and Mortality Committee. Outcomes ascertainment and adjudication methods in the Women's Health Initiative. Ann Epidemiol. 2003; 13 (9 Suppl) S122-8.
34. Jackson RD, LaCroix AZ, Cauley JA, McGowan J., The Women's Health Initiative calcium-vitamin D trial: overview and baseline characteristics of participants. Ann Epidemiol. 2003; 13 (9 Suppl) S98-106.
35. Patterson RE, Kristal AR, Tinker LF, Carter RA, Bolton MP, Agurs-Collins T., Measurement characteristics of the Women's Health Initiative food frequency questionnaire. Ann Epidemiol. 1999; 9 (3): 178-87.
36. Jackson RD, LaCroix AZ, Gass M, Wallace RB, Robbins J, Lewis CE, Bassford T, Beresford SA, Black HR, Blanchette P, Bonds DE, Brunner RL, Brzyski RG, Caan B, Cauley JA, Chlebowski RT, Cummings SR, Granek I, Hays J, Heiss G, Hendrix SL, Howard BV, Hsia J, Hubbell FA, Johnson KC, Judd H, Kotchen JM, Kuller LH, Langer RD, Lasser NL, Limacher MC, Ludlam S, Manson JE, Margolis KL, McGowan J, Ockene JK, O'Sullivan MJ, Phillips L, Prentice RL, Sarto GE, Stefanick ML, Van Horn L, Wactawski-Wende J, Whitlock E, Anderson GL, Assaf AR., Barad D; Women's Health Initiative Investigators. Calcium plus Vitamin D supplementation and the risk of fractures. N Engl J Med. 2006; 354 (7): 669-83. DOI: 10.1056/NEJMoa055218
37. Robbins J, Aragaki AK, Kooperberg C, Watts N, Wactawski-Wende J, Jackson RD, LeBoff MS, Lewis CE, Chen Z, Stefanick ML, Cauley J., Factors associated, with 5-year, risk of, hip fracture, in postmenopausal, women. JAMA. 2007; 298 (20): 2389-98. DOI: 10.1001/jama.298.20.2389
38. Anderson GL, Manson J, Wallace R, Lund B, Hall D, Davis S, Shumaker S, Wang CY, Stein E, Prentice RL., Implementation of the women's health initiative study design. Ann Epidemiol. 2003; 13 (9 Suppl) S5-17.
39. Harris WS, Lemke SL, Hansen SN, Goldstein DA, DiRienzo MA, Su H, Nemeth MA, Taylor ML, Ahmed G, George C., Stearidonic acid-enriched soybean oil increased the omega-3 index, an emerging cardiovascular risk marker. Lipids. 2008; 43 (9): 805-11.
40. Belury MA, Kempa-Steczko A., Conjugated linoleic acid modulates hepatic lipid composition in mice. Lipids. 1997; 32 (2): 199-204. Cited. in: PubMed; PMID. 9075211.
41. U.S., Department of Agriculture, ARS, Beltsville Human Nutrition Research Center, Food Surveys Research Group and U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics. What We Eat in America, NHANES 2007-2008 [Internet]. Washington, DC: Agricultural Research Service, U.S. Department of Agriculture [updated 2012 Jul 16; cited. 2012 Sep 26]. Available from: http://www.ars.usda.gov/Services/ docs.htm?docid=18349.
42. Magnusardottir AR, Skuladottir GV., Effects of storage time and added antioxidant on fatty acid composition of red blood cells at -20 degrees C. Lipids. 2006; 41 (4): 401-14.
43. Hodson L, Skeaff CM, Wallace AJ, Arribas GL., Stability of plasma and erythrocyte fatty acid composition during cold storage. Clin Chim Acta. 2002; 321 (1-2): 63-7.
44. Sun Q, Ma J, Campos H, Rexrode KM, Albert CM, Mozaffarian D, Hu FB., Blood concentrations of individual long-chain n-3 fatty acids and risk of nonfatal myocardial infarction. Am J Clin Nutr. 2008; 88 (1): 216-23.
45. Sands SA, Reid KJ, Windsor SL, Harris WS., The impact of age, body mass index, and fish intake on the EPA and DHA content of human erythrocytes. Lipids. 2005; 40 (4): 343-7.
46. Itomura M, Fujioka S, Hamazaki K, Kobayashi K, Nagasawa T, Sawazaki S, Kirihara Y, Hamazaki T., Factors influencing EPA + DHA levels in red blood cells in Japan. In Vivo. 2008; 22 (1): 131-5.
47. Farina EK, Kiel DP, Roubenoff R, Schaefer EJ, Cupples LA, Tucker KL., Plasma phosphatidylcholine concentrations of polyunsaturated fatty acids are differentially associated with hip bone mineral density and hip fracture in older adults: the Framingham Osteoporosis Study. J Bone Miner Res. 2012; 27 (5): 1222-30. Epub. 2012 Mar 07. DOI: 10.1002/jbmr.1581
48. Hodson L, McQuaid SE, Karpe F, Frayn KN, Fielding BA., Differences in partitioning of meal fatty acids into blood lipid fractions: a comparison of linoleate, oleate, and palmitate. Am J Physiol. 2009; 296 (1): E64-71.
49. Martinez-Ramirez MJ, Palma S, Martinez-Gonzalez MA, Delgado-Martinez AD, de la Fuente C, Delgado-Rodriguez M., Dietary fat intake and the risk of osteoporotic fractures in the elderly. Eur J Clin Nutr. 2007; 61 (9): 1114-20.
50. Arterburn LM, Hall EB, Oken H., Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr. 2006; 83 (6): S1467-76.
51. Schaeffer L, Gohlke H, Müller M, Heid IM, Palmer LJ, Kompauer I, Demmelmair H, Illig T, Koletzko B, Heinrich J., Common genetic variants of the FADS1 FADS2 gene cluster and their reconstructed haplotypes are associated with the fatty acid composition in phospholipids. Hum Mol Genet. 2006; 15 (11): 1745-56.
52. Malerba G, Schaeffer L, Xumerle L, Klopp N, Trabetti E, Biscuola M, Cavallari U, Galavotti R, Martinelli N, Guarini P, Girelli D, Olivieri O, Corrocher R, Heinrich J, Pignatti PF, Illig T., SNPs of the FADS gene cluster are associated with polyunsaturated fatty acids in a cohort of patients with cardiovascular disease. Lipids. 2008; 43 (4): 289-99.
53. Brossard N, Croset M, Pachiaudi C, Riou JP, Tayot JL, Lagarde M., Retroconversion and metabolism of [13C]22:6n-3 in humans and rats after intake of a single dose of [13C]22:6n-3-triacylglycerols. Am J Clin Nutr. 1996; 64 (4): 577-86.
54. Simopoulos AP., The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med (Maywood). 2008; 233 (6): 674-88. DOI: 10.3181/0711-mr-311
55. Weiss LA, Barrett-Connor E, von Muhlen D., Ratio of n-6 to n-3 fatty acids and bone mineral density in older adults: the Rancho Bernardo Study. Am J Clin Nutr. 2005; 81 (4): 934-8.
56. Hodson L, Skeaff CM, Fielding BA., Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res. 2008; 47 (5): 348-80.
57. Sampath H, Ntambi JM., The fate and intermediary metabolism of stearic acid. Lipids. 2005; 40 (12): 1187-91.
58. Moon HJ, Kim TH, Byun DW, Park Y., Positive correlation between erythrocyte levels of n-3 polyunsaturated fatty acids and bone mass in postmenopausal Korean women with osteoporosis. Ann Nutr Metab. 2012; 60 (2): 146-53. DOI: 10.1159/000337302
59. Farina EK, Kiel DP, Roubenoff R, Schaefer EJ, Cupples LA, Tucker KL., Protective effects of fish intake and interactive effects of long-chain polyunsaturated fatty acid intakes on hip bone mineral density in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr. 2011; 93 (5): 1142-51.
60. Patel PS, Sharp SJ, Jansen E, Luben RN, Khaw KT, Wareham NJ, Forouhi NG., Fatty acids measured in plasma and erythrocyte-membrane phospholipids and derived by food-frequency questionnaire and the risk of new-onset type 2 diabetes: a pilot study in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk cohort. Am J Clin Nutr. 2010; 92 (5): 1214-22.
61. Timbo BB, Ross MP, McCarthy PV, Lin CT., Dietary supplements in a national survey: Prevalence of use and reports of adverse events. J Am Diet Assoc. 2006; 106 (12): 1966-74.
62. Artz MB, Harnack LJ, Duval SJ, Armstrong C, Arnett DK, Luepker RV., Use of nonprescription medications for perceived cardiovascular health. Am J Prev Med. 2006; 30 (1): 78-81.
63. Qato DM, Alexander GC, Conti RM, Johnson M, Schumm P, Lindau ST., Use of, prescription over-the-counter, medications dietary, supplements among, older adults, in the, United States. JAMA. 2008; 300 (24): 2867-78.