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Published in: Nutrition & Metabolism 1/2011

Open Access 01-12-2011 | Research

Long-term aerobic exercise and omega-3 supplementation modulate osteoporosis through inflammatory mechanisms in post-menopausal women: a randomized, repeated measures study

Authors: Bakhtyar Tartibian, Behzad Hajizadeh Maleki, Jill Kanaley, Karim Sadeghi

Published in: Nutrition & Metabolism | Issue 1/2011

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Abstract

Background

Evidence indicates that dietary fats and physical activity influence bone health. The purpose of this study was to examine the effects of long-term aerobic exercise and omega-3 (N-3) supplementation on serum inflammatory markers, bone mineral density (BMD), and bone biomarkers in post-menopausal women.

Methods

Seventy-nine healthy sedentary post-menopausal women aged 58-78 years participated in this study. Subjects were randomized to one of 4 groups: exercise + supplement (E+S, n = 21), exercise (E, n = 20), supplement (S, n = 20), and control (Con, n = 18) groups. The subjects in the E+S and E groups performed aerobic exercise training (walking and jogging) up to 65% of HRmax, three times a week for 24 weeks. Subjects in the E+S and S groups consumed 1000 mg/d N-3 for 24 weeks. The lumbar spine (L2-L4) and femoral neck BMD, serum tumor necrosis factor (TNF) α, interleukin (IL) 6, prostaglandin (PG) E2, estrogen, osteocalcin, 1, 25-dihydroxyvitamin D3 (1, 25 Vit D), C-telopeptide (CTX), parathyroid hormone (PTH) and calcitonin (CT) were measured at baseline, the end of week 12 and 24.

Results

Serum estrogen, osteocalcin, 1, 25 Vit D, CT, L2-L4 and femoral neck BMD measures increased (P < 0.05) and the serum CTX, PTH, TNF-α, IL-6, and PGE2 decreased (P < 0.05) in E + S group after the 24 wk intervention but not in the E or S intervention groups. L2-L4 and femoral neck BMD, estrogen, osteocalcin, and CT were negatively (P < 0.05) correlated with TNF-α and PGE2. PTH and CT were correlated positively and negatively with IL-6, respectively (P < 0.05).

Conclusions

The present study demonstrates that long-term aerobic exercise training plus N-3 supplementation have a synergistic effect in attenuating inflammation and augmenting BMD in post-menopausal osteoporosis.
Literature
1.
go back to reference Mori S: Mechanism of bone metabolism: The effects of exercise on bone movement. J Clin Sports Med 1994, 11: 1233-1238. Mori S: Mechanism of bone metabolism: The effects of exercise on bone movement. J Clin Sports Med 1994, 11: 1233-1238.
2.
go back to reference Guillemant JC, Accarie G, Peres S, Guillemant A: Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif Tissue Int 2004, 74: 407-414. 10.1007/s00223-003-0070-0CrossRef Guillemant JC, Accarie G, Peres S, Guillemant A: Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif Tissue Int 2004, 74: 407-414. 10.1007/s00223-003-0070-0CrossRef
3.
go back to reference De Martinis M, Di Benedetto MC, Mengoli LP, Ginaldi L: Senile osteoporosis: is it an immune-mediated disease? Inflamm Res 2006, 55: 399-404. 10.1007/s00011-006-6034-xCrossRef De Martinis M, Di Benedetto MC, Mengoli LP, Ginaldi L: Senile osteoporosis: is it an immune-mediated disease? Inflamm Res 2006, 55: 399-404. 10.1007/s00011-006-6034-xCrossRef
4.
go back to reference Ginaldi L, Di Benedetto MC, De Martinis M: Osteoporosis, inflammation and ageing. Immun Aging 2005, 2: 14. 10.1186/1742-4933-2-14CrossRef Ginaldi L, Di Benedetto MC, De Martinis M: Osteoporosis, inflammation and ageing. Immun Aging 2005, 2: 14. 10.1186/1742-4933-2-14CrossRef
5.
go back to reference Kwan TS, Padrines M, Theoleyre S, Heymann D, Fortun Y: IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev 2004, 15: 49-60. 10.1016/j.cytogfr.2003.10.005CrossRef Kwan TS, Padrines M, Theoleyre S, Heymann D, Fortun Y: IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev 2004, 15: 49-60. 10.1016/j.cytogfr.2003.10.005CrossRef
6.
go back to reference Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB: Inflammatory markers and incident fracture risk in older men and women: the health aging and body composition study. J Bone Miner Res 2007, 22: 1088-1095. 10.1359/jbmr.070409CrossRef Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB: Inflammatory markers and incident fracture risk in older men and women: the health aging and body composition study. J Bone Miner Res 2007, 22: 1088-1095. 10.1359/jbmr.070409CrossRef
7.
go back to reference Muller B: Cytokine imbalance in non-immunological chronic disease. Cytokine 2002, 18: 334-339. 10.1006/cyto.2002.0882CrossRef Muller B: Cytokine imbalance in non-immunological chronic disease. Cytokine 2002, 18: 334-339. 10.1006/cyto.2002.0882CrossRef
8.
go back to reference Manolagas SC: Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000, 21: 115-137. 10.1210/er.21.2.115 Manolagas SC: Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000, 21: 115-137. 10.1210/er.21.2.115
9.
go back to reference Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR: Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 1986, 319: 516-518. 10.1038/319516a0CrossRef Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR: Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 1986, 319: 516-518. 10.1038/319516a0CrossRef
10.
go back to reference Raisz LG, Rodan GA: Pathogenesis of osteoporosis. Endocrinol Metab Clin N Am 2003, 32: 15-24. 10.1016/S0889-8529(02)00055-5CrossRef Raisz LG, Rodan GA: Pathogenesis of osteoporosis. Endocrinol Metab Clin N Am 2003, 32: 15-24. 10.1016/S0889-8529(02)00055-5CrossRef
11.
go back to reference Raisz LG: Physiology and pathophysiology of bone remodeling. Clin Chem 1999, 45: 1353-1358. Raisz LG: Physiology and pathophysiology of bone remodeling. Clin Chem 1999, 45: 1353-1358.
12.
go back to reference Tartibian B, Hajizadeh BM, Abbasi A: The calciotropic hormone response to omega-3 supplementation during longterm weight-bearing exercise training in post menopausal women. J Sport Sci Med 2010, 9: 245-252. Tartibian B, Hajizadeh BM, Abbasi A: The calciotropic hormone response to omega-3 supplementation during longterm weight-bearing exercise training in post menopausal women. J Sport Sci Med 2010, 9: 245-252.
13.
go back to reference Watkins BA, Li Y, Lippman HE, Feng S: Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism. Prostaglandins Leukot Essent Fatty Acids 2003, 68: 387-398. 10.1016/S0952-3278(03)00063-2CrossRef Watkins BA, Li Y, Lippman HE, Feng S: Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism. Prostaglandins Leukot Essent Fatty Acids 2003, 68: 387-398. 10.1016/S0952-3278(03)00063-2CrossRef
14.
go back to reference Terano T: Effect of omega 3 polyunsaturated fatty acid ingestion on bone metabolism and osteoporosis. World Rev Nutr Diet 2001, 88: 141-147.CrossRef Terano T: Effect of omega 3 polyunsaturated fatty acid ingestion on bone metabolism and osteoporosis. World Rev Nutr Diet 2001, 88: 141-147.CrossRef
15.
go back to reference Amy EG, Penny MK, Kristen FH, Guixiang Z, Sheila GW, Rebecca LC: An increase in dietary N-3 fatty acids decreases a marker of bone resorption in humans. Nutrition Journal 2007, 6: 2. 10.1186/1475-2891-6-2CrossRef Amy EG, Penny MK, Kristen FH, Guixiang Z, Sheila GW, Rebecca LC: An increase in dietary N-3 fatty acids decreases a marker of bone resorption in humans. Nutrition Journal 2007, 6: 2. 10.1186/1475-2891-6-2CrossRef
16.
go back to reference Bruce A, Watkins T, Yong Li, 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: 282-289. 10.1016/j.jnutbio.2005.05.012CrossRef Bruce A, Watkins T, Yong Li, 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: 282-289. 10.1016/j.jnutbio.2005.05.012CrossRef
17.
go back to reference Shen CL, James K, Yeh JK, Rasty J, Li Y, Bruce A: Protective effect of dietary long-chain N-3 polyunsaturated fatty acids on bone loss in gonad-intact middle-aged male rats. British J Nutr 2006, 95: 462-468. 10.1079/BJN20051664CrossRef Shen CL, James K, Yeh JK, Rasty J, Li Y, Bruce A: Protective effect of dietary long-chain N-3 polyunsaturated fatty acids on bone loss in gonad-intact middle-aged male rats. British J Nutr 2006, 95: 462-468. 10.1079/BJN20051664CrossRef
18.
go back to reference Philip CC: N-3 polyunsaturated fatty acids, inflammation, and inflammatory Diseases. Am J Clin Nutr 2006, 83: 1505-1519. Philip CC: N-3 polyunsaturated fatty acids, inflammation, and inflammatory Diseases. Am J Clin Nutr 2006, 83: 1505-1519.
19.
go back to reference Yamazaki S, Ichimura S, Iwamoto J, Takeda T, Toyama Y: Effect of walking exercise on bone metabolism in post-menopausal women with osteopenia/osteoporosis. J Bone Miner Metab 2004, 22: 500-508.CrossRef Yamazaki S, Ichimura S, Iwamoto J, Takeda T, Toyama Y: Effect of walking exercise on bone metabolism in post-menopausal women with osteopenia/osteoporosis. J Bone Miner Metab 2004, 22: 500-508.CrossRef
20.
go back to reference Creighton DL, Amy MorganL, Debra B, Brolinson PG: Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol 2001, 90: 565-570. Creighton DL, Amy MorganL, Debra B, Brolinson PG: Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol 2001, 90: 565-570.
21.
go back to reference Iwamoto J, Takeda T, Ichimura S: Effects of exercise training and detraining on BMD in post-menopausal women with osteoprosis. J Ortho Sci 2001, 6: 128-132. 10.1007/s007760100059CrossRef Iwamoto J, Takeda T, Ichimura S: Effects of exercise training and detraining on BMD in post-menopausal women with osteoprosis. J Ortho Sci 2001, 6: 128-132. 10.1007/s007760100059CrossRef
22.
go back to reference Menkes A, Mazel S, Redmond RA, Koffler K, Libanti CR, Gundberg CM, Zizic TM, Hagberg JM, Pratley RE, Hurley BF: Strength training increases regional bone mineral density and bone remodeling in middle-aged and older men. J Appl Physiol 1993, 74: 2478-2484. Menkes A, Mazel S, Redmond RA, Koffler K, Libanti CR, Gundberg CM, Zizic TM, Hagberg JM, Pratley RE, Hurley BF: Strength training increases regional bone mineral density and bone remodeling in middle-aged and older men. J Appl Physiol 1993, 74: 2478-2484.
23.
go back to reference Rockwell JC, Sorensen DM, Baker S, Leahey J, Stock L, Michaels J, Baran DT: Weight training decreases vertebral bone density in premenopausal women: a prospective study. J Clin Endocrinol Metab 1990, 71: 988-993. 10.1210/jcem-71-4-988CrossRef Rockwell JC, Sorensen DM, Baker S, Leahey J, Stock L, Michaels J, Baran DT: Weight training decreases vertebral bone density in premenopausal women: a prospective study. J Clin Endocrinol Metab 1990, 71: 988-993. 10.1210/jcem-71-4-988CrossRef
24.
go back to reference Nelson ME, Fiatarone MA, Morganti CM, Trice I, Greenberg RA, Evans WJ: Effects of high-intensity strength training on multiple risk factors for osteoporotic fractures: a randomized controlled trial. J Am Med Assoc 1994, 272: 1909-1914. 10.1001/jama.272.24.1909CrossRef Nelson ME, Fiatarone MA, Morganti CM, Trice I, Greenberg RA, Evans WJ: Effects of high-intensity strength training on multiple risk factors for osteoporotic fractures: a randomized controlled trial. J Am Med Assoc 1994, 272: 1909-1914. 10.1001/jama.272.24.1909CrossRef
25.
go back to reference Iwamoto J, Shimamur C, Taked T, Hitoshi A, Ichimur S, Sato Y, Toyam Y: The effects of exercise on bone mass, bone metabolism, and calciotropic hormones in young growing rats. J Bone Miner Metab 2004, 22: 26-31. 10.1007/s00774-003-0443-5CrossRef Iwamoto J, Shimamur C, Taked T, Hitoshi A, Ichimur S, Sato Y, Toyam Y: The effects of exercise on bone mass, bone metabolism, and calciotropic hormones in young growing rats. J Bone Miner Metab 2004, 22: 26-31. 10.1007/s00774-003-0443-5CrossRef
26.
go back to reference Yeh JK, Aloia JF: Effect of physical activity on calciotropic hormones and calcium balance in rats. Am J Physiol 1990, 258: 263-268. Yeh JK, Aloia JF: Effect of physical activity on calciotropic hormones and calcium balance in rats. Am J Physiol 1990, 258: 263-268.
27.
go back to reference Alev A, Yurtkuran M: Evaluation of hormonal response and ultrasonic changes in the heel bone by aquatic exercise in sedentary post-menopausal women. Ame J Physic Med Rehab 2003, 82: 942-949. 10.1097/01.PHM.0000098039.58584.59CrossRef Alev A, Yurtkuran M: Evaluation of hormonal response and ultrasonic changes in the heel bone by aquatic exercise in sedentary post-menopausal women. Ame J Physic Med Rehab 2003, 82: 942-949. 10.1097/01.PHM.0000098039.58584.59CrossRef
28.
go back to reference James OJ, Kleppinger A, Kenny JAS, Biskup B, Glenn M: Home-based resistance training improves femoral bone mineral density in women on hormone therapy. Osteoporos Int 2005, 16: 1096-1108. 10.1007/s00198-004-1816-xCrossRef James OJ, Kleppinger A, Kenny JAS, Biskup B, Glenn M: Home-based resistance training improves femoral bone mineral density in women on hormone therapy. Osteoporos Int 2005, 16: 1096-1108. 10.1007/s00198-004-1816-xCrossRef
29.
go back to reference Ashizawa N, Ouchi G, Fujimara R, Yoshida Y, Tokuyama K, Suzuki M: Effects of a single bout of resistance exercise on calcium and bone metabolism in untrained young males. Calcif Tiss Int 1998, 62: 104-108. 10.1007/s002239900402CrossRef Ashizawa N, Ouchi G, Fujimara R, Yoshida Y, Tokuyama K, Suzuki M: Effects of a single bout of resistance exercise on calcium and bone metabolism in untrained young males. Calcif Tiss Int 1998, 62: 104-108. 10.1007/s002239900402CrossRef
30.
go back to reference Prince RL, Smith M, Dick IM, Price RI, Webb PG, Henderson NK, Harris MM: Prevention of post-menopausal osteoporosis: a comparative study of exercise, calcium supplementation, and hormone-replacement therapy. N Engl J Med 1991, 325: 1189-1195. 10.1056/NEJM199110243251701CrossRef Prince RL, Smith M, Dick IM, Price RI, Webb PG, Henderson NK, Harris MM: Prevention of post-menopausal osteoporosis: a comparative study of exercise, calcium supplementation, and hormone-replacement therapy. N Engl J Med 1991, 325: 1189-1195. 10.1056/NEJM199110243251701CrossRef
31.
go back to reference Campbell PT, Campbell KL, Wener MH, Wood BL, Potter JD, Mctiernan A, Ulrich CM: A Yearlong Exercise Intervention Decreases CRP among Obese Post-menopausal Women. Med Sci Sport Exer 2009, 41: 1533-1539. 10.1249/MSS.0b013e31819c7febCrossRef Campbell PT, Campbell KL, Wener MH, Wood BL, Potter JD, Mctiernan A, Ulrich CM: A Yearlong Exercise Intervention Decreases CRP among Obese Post-menopausal Women. Med Sci Sport Exer 2009, 41: 1533-1539. 10.1249/MSS.0b013e31819c7febCrossRef
32.
go back to reference Kohut ML, McCann DA, Russell DW, Konopka DN, Cunnick JE, Franke WD, Castillo MC, Reighard AE, Vanderah E: Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of beta-blockers, BMI, and psychosocial factors in older adults. Brain Behav Immun 2006, 20: 201-209. 10.1016/j.bbi.2005.12.002CrossRef Kohut ML, McCann DA, Russell DW, Konopka DN, Cunnick JE, Franke WD, Castillo MC, Reighard AE, Vanderah E: Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of beta-blockers, BMI, and psychosocial factors in older adults. Brain Behav Immun 2006, 20: 201-209. 10.1016/j.bbi.2005.12.002CrossRef
33.
go back to reference Kasapis C, Thompson PD: The Effects of Physical Activity on Serum C - reactive protein and Inflammatory Markers: A Systematic Review. J Am Coll Cardiol 2005, 45: 1563-1569. 10.1016/j.jacc.2004.12.077CrossRef Kasapis C, Thompson PD: The Effects of Physical Activity on Serum C - reactive protein and Inflammatory Markers: A Systematic Review. J Am Coll Cardiol 2005, 45: 1563-1569. 10.1016/j.jacc.2004.12.077CrossRef
34.
go back to reference Bruce RA, Hornsten TR: Exercise stress testing in evaluation of patients with ischemic heart disease. Prog Cardiovas Dis 1969, 11: 371-390. 10.1016/0033-0620(69)90027-9CrossRef Bruce RA, Hornsten TR: Exercise stress testing in evaluation of patients with ischemic heart disease. Prog Cardiovas Dis 1969, 11: 371-390. 10.1016/0033-0620(69)90027-9CrossRef
35.
go back to reference Washburn RA, Ficker JL: Physical activity scale for the elderly (PASE): the relationship with activity measured by a portable accelerometer. J Sport Med Phys Fit 1999, 39: 336-340. Washburn RA, Ficker JL: Physical activity scale for the elderly (PASE): the relationship with activity measured by a portable accelerometer. J Sport Med Phys Fit 1999, 39: 336-340.
36.
go back to reference The Ministry of Science and Technology: The fifth revision of the standard table of food composition in Japan. Kagawa Nutrition University Publishing, Tokyo, Japan; 2004. The Ministry of Science and Technology: The fifth revision of the standard table of food composition in Japan. Kagawa Nutrition University Publishing, Tokyo, Japan; 2004.
37.
go back to reference Tartibian B, Hajizadeh BM, Abbasi A: The effects of omega-3 supplementation on pulmonary function of young wrestlers during intensive training. J Sci Med Sport 2010, 13: 281-286. 10.1016/j.jsams.2008.12.634CrossRef Tartibian B, Hajizadeh BM, Abbasi A: The effects of omega-3 supplementation on pulmonary function of young wrestlers during intensive training. J Sci Med Sport 2010, 13: 281-286. 10.1016/j.jsams.2008.12.634CrossRef
38.
go back to reference Lin L, Hsieh L, Sandy S: Effects of strength and endurance exercise on calcium-regulating hormones between different levels of physical activity. J Mech Med Biol 2005, 5: 267-275. 10.1142/S0219519405001461CrossRef Lin L, Hsieh L, Sandy S: Effects of strength and endurance exercise on calcium-regulating hormones between different levels of physical activity. J Mech Med Biol 2005, 5: 267-275. 10.1142/S0219519405001461CrossRef
39.
go back to reference Iwamoto J, Takeda T, Ichimura S: Effects of exercise on bone mineral density in mature osteopenic rats. J Bone Miner Res 1998, 13: 1308-1317. 10.1359/jbmr.1998.13.8.1308CrossRef Iwamoto J, Takeda T, Ichimura S: Effects of exercise on bone mineral density in mature osteopenic rats. J Bone Miner Res 1998, 13: 1308-1317. 10.1359/jbmr.1998.13.8.1308CrossRef
40.
go back to reference Yeh JK, Liu CC, Aloia JF: Additive effect of treadmill exercise and 17 beta-estradiol replacement on prevention of tibial bone loss in adult ovariectomized rats. J Bone Miner Res 1993, 8: 677-683.CrossRef Yeh JK, Liu CC, Aloia JF: Additive effect of treadmill exercise and 17 beta-estradiol replacement on prevention of tibial bone loss in adult ovariectomized rats. J Bone Miner Res 1993, 8: 677-683.CrossRef
41.
go back to reference Yeh JK, Aloia JF, Yasumura S: Effect of physical activity on calcium and phosphorus metabolism in the rat. Am J Physiol 1989, 256: 1-6. Yeh JK, Aloia JF, Yasumura S: Effect of physical activity on calcium and phosphorus metabolism in the rat. Am J Physiol 1989, 256: 1-6.
42.
go back to reference McTiernan A, Shelley S, Tworoger CM, Yutaka Y, Irwin ML, Rajan KB, Sorensen B, Rudolph RE, Bowen D, Stanczyk FZ, Potter JD, Schwartz RS: Effect of Exercise on Serum Estrogens in Post-menopausal Women: A 12-Month Randomized Clinical Trial. Cancer Research 2004, 64: 2923-2928. 10.1158/0008-5472.CAN-03-3393CrossRef McTiernan A, Shelley S, Tworoger CM, Yutaka Y, Irwin ML, Rajan KB, Sorensen B, Rudolph RE, Bowen D, Stanczyk FZ, Potter JD, Schwartz RS: Effect of Exercise on Serum Estrogens in Post-menopausal Women: A 12-Month Randomized Clinical Trial. Cancer Research 2004, 64: 2923-2928. 10.1158/0008-5472.CAN-03-3393CrossRef
43.
go back to reference Turner RT, Lawrence RB, Spelsberg TC: Skeletal effects of estrogen. Endocrine Reviews 1994, 15: 275-300. Turner RT, Lawrence RB, Spelsberg TC: Skeletal effects of estrogen. Endocrine Reviews 1994, 15: 275-300.
44.
go back to reference Weryha G, Leclere J: Paracrine regulation of bone remodeling. Hormone Research 1995, 43: 69-75. 10.1159/000184240CrossRef Weryha G, Leclere J: Paracrine regulation of bone remodeling. Hormone Research 1995, 43: 69-75. 10.1159/000184240CrossRef
45.
go back to reference Debra A, Bemben L, Nicole L: The Independent and Additive Effects of Exercise Training and Estrogen on Bone Metabolism. J Strength Condit Res 2000, 14: 114-120. Debra A, Bemben L, Nicole L: The Independent and Additive Effects of Exercise Training and Estrogen on Bone Metabolism. J Strength Condit Res 2000, 14: 114-120.
46.
go back to reference Duursma SA, Raymakers JA, Boeroom FTJ, Scheven BAA: Estrogen and bone metabolism. Obstet Gynecol 1991, 47: 38-44. Duursma SA, Raymakers JA, Boeroom FTJ, Scheven BAA: Estrogen and bone metabolism. Obstet Gynecol 1991, 47: 38-44.
47.
go back to reference Bruunsgaard H: Physical activity and modulation of systemic low-level inflammation. J Leukocyte Biol 2005, 78: 819-835. 10.1189/jlb.0505247CrossRef Bruunsgaard H: Physical activity and modulation of systemic low-level inflammation. J Leukocyte Biol 2005, 78: 819-835. 10.1189/jlb.0505247CrossRef
48.
go back to reference Venkatraman JT, Chu WC: Effects of dietary omega-3 and omega- 6 lipids and vitamin E on serum cytokines, lipid mediators and anti-DNA antibodies in a mouse model for rheumatoid arthritis. J Am Coll Nutr 1999, 18: 602-613.CrossRef Venkatraman JT, Chu WC: Effects of dietary omega-3 and omega- 6 lipids and vitamin E on serum cytokines, lipid mediators and anti-DNA antibodies in a mouse model for rheumatoid arthritis. J Am Coll Nutr 1999, 18: 602-613.CrossRef
49.
go back to reference Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ: The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in N-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr 1996, 63: 116-122. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ: The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in N-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr 1996, 63: 116-122.
50.
go back to reference Gallai V, Sarchielli P, Trequattrini A, Franceschini M, Floridi A, Firenze C, Alberti A, Di Benedetto D, Stragliotto E: Cytokine secretion and eicosanoid production in the peripheral blood mononuclear cells of MS patients undergoing dietary supplementation with N-3 polyunsaturated fatty acids. J Neuroimmunol 1995, 56: 143-153. 10.1016/0165-5728(94)00140-JCrossRef Gallai V, Sarchielli P, Trequattrini A, Franceschini M, Floridi A, Firenze C, Alberti A, Di Benedetto D, Stragliotto E: Cytokine secretion and eicosanoid production in the peripheral blood mononuclear cells of MS patients undergoing dietary supplementation with N-3 polyunsaturated fatty acids. J Neuroimmunol 1995, 56: 143-153. 10.1016/0165-5728(94)00140-JCrossRef
51.
go back to reference Tartibian B, Hajizadeh BM, Abbasi A: Omega-3 Fatty Acids Supplementation Attenuates Inflammatory Markers After Eccentric Exercise in Untrained Men. Clin J Sport Med 2011, 21: 131-137. 10.1097/JSM.0b013e31820f8c2fCrossRef Tartibian B, Hajizadeh BM, Abbasi A: Omega-3 Fatty Acids Supplementation Attenuates Inflammatory Markers After Eccentric Exercise in Untrained Men. Clin J Sport Med 2011, 21: 131-137. 10.1097/JSM.0b013e31820f8c2fCrossRef
52.
go back to reference Meydani SN, Lichtenstein AH, Cornwall S, Meydani M, Goldin BR, Rasmussen H, Dinarello CA, Schaefer EJ: Immunologic effects of national cholesterol education panel step-2 diets with and without fish-derived N-3 fatty acid enrichment. J Clin Invest 1993, 92: 105-113. 10.1172/JCI116537CrossRef Meydani SN, Lichtenstein AH, Cornwall S, Meydani M, Goldin BR, Rasmussen H, Dinarello CA, Schaefer EJ: Immunologic effects of national cholesterol education panel step-2 diets with and without fish-derived N-3 fatty acid enrichment. J Clin Invest 1993, 92: 105-113. 10.1172/JCI116537CrossRef
53.
go back to reference Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S: The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochimica et Biophysica Acta 2011, 1813: 878-888. 10.1016/j.bbamcr.2011.01.034CrossRef Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S: The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochimica et Biophysica Acta 2011, 1813: 878-888. 10.1016/j.bbamcr.2011.01.034CrossRef
54.
go back to reference Atkinson C, Malarkey WB, Glaser R: Chronic stress and age-related increases in the proinflammatory cytokine IL-6. The National Academy of Sciences of the United States of America 2003, 100: 9090-9095. 10.1073/pnas.1531903100CrossRef Atkinson C, Malarkey WB, Glaser R: Chronic stress and age-related increases in the proinflammatory cytokine IL-6. The National Academy of Sciences of the United States of America 2003, 100: 9090-9095. 10.1073/pnas.1531903100CrossRef
55.
go back to reference Peake JM, Suzuki K, Hordern M, Wilson G, Nosaka K, Coombs JS: Plasma cytokine changes in relation to exercise intensity and muscle damage. European Journal of Applied Physiology 2005, 95: 514-521. 10.1007/s00421-005-0035-2CrossRef Peake JM, Suzuki K, Hordern M, Wilson G, Nosaka K, Coombs JS: Plasma cytokine changes in relation to exercise intensity and muscle damage. European Journal of Applied Physiology 2005, 95: 514-521. 10.1007/s00421-005-0035-2CrossRef
56.
go back to reference Mitnick MA, Grey A, Masiukiewicz U, Bartkiewicz M, Rios-Velez L, Friedman S, Xu L, Horowitz MC, Insogna K: Parathyroid hormone induces hepatic production of bioactive interleukin-6 and its soluble receptor. Am J Physiol Endocrinol Metab 2001, 280: 405-412. Mitnick MA, Grey A, Masiukiewicz U, Bartkiewicz M, Rios-Velez L, Friedman S, Xu L, Horowitz MC, Insogna K: Parathyroid hormone induces hepatic production of bioactive interleukin-6 and its soluble receptor. Am J Physiol Endocrinol Metab 2001, 280: 405-412.
57.
go back to reference Bismar H, Diel I, Ziegler R, Pfeilschifter J: Increased cytokine secretion by human bone marrow cells after menopause or discontinuation of estrogen replacement. J Clin Endocrinol Metab 1995, 80: 3351-3555. 10.1210/jc.80.11.3351 Bismar H, Diel I, Ziegler R, Pfeilschifter J: Increased cytokine secretion by human bone marrow cells after menopause or discontinuation of estrogen replacement. J Clin Endocrinol Metab 1995, 80: 3351-3555. 10.1210/jc.80.11.3351
58.
go back to reference Weitzmann MN, Pacifici R: Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 2006, 116: 1186-1194. 10.1172/JCI28550CrossRef Weitzmann MN, Pacifici R: Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 2006, 116: 1186-1194. 10.1172/JCI28550CrossRef
59.
go back to reference Sahin G, Ozturk C, Bagis S, Cimen OB, Erdogan C: Correlation of Serum Cytokine Levels with Axial Bone Mineral Density. Singapore Med J 2002, 43: 576-578. Sahin G, Ozturk C, Bagis S, Cimen OB, Erdogan C: Correlation of Serum Cytokine Levels with Axial Bone Mineral Density. Singapore Med J 2002, 43: 576-578.
60.
go back to reference Weinhold B, Ruther U: Interleukin-6-dependent and -independent regulation of the human C-reactive protein gene. Biochem J 1997, 327: 425-429.CrossRef Weinhold B, Ruther U: Interleukin-6-dependent and -independent regulation of the human C-reactive protein gene. Biochem J 1997, 327: 425-429.CrossRef
61.
go back to reference Yoshida N, Ikemoto S, Narita K, Sugimura K, Wada S, Yasumoto R, Kishimoto T, Nakatani T: Interleukin-6, tumour necrosis factor alpha and interleukin-1beta in patients with renal cell carcinoma. Br J Cancer 2002, 86: 1396-1400. 10.1038/sj.bjc.6600257CrossRef Yoshida N, Ikemoto S, Narita K, Sugimura K, Wada S, Yasumoto R, Kishimoto T, Nakatani T: Interleukin-6, tumour necrosis factor alpha and interleukin-1beta in patients with renal cell carcinoma. Br J Cancer 2002, 86: 1396-1400. 10.1038/sj.bjc.6600257CrossRef
62.
go back to reference Gowen M, Mundy GR: Actions of recombinant interleukin 1, interleukin 2, and interferon-gamma on bone resorption in vitro. J Immunol 1986, 136: 2478-2482. Gowen M, Mundy GR: Actions of recombinant interleukin 1, interleukin 2, and interferon-gamma on bone resorption in vitro. J Immunol 1986, 136: 2478-2482.
63.
go back to reference Salamone LM, Whiteside T, Friberg D, Epstein RS, Kuller LH, Cauley JA: Cytokine production and bone mineral density at the lumbar spine and femoral neck in premenopausal women. Calcif Tissue Int 1998, 63: 466-470. 10.1007/s002239900559CrossRef Salamone LM, Whiteside T, Friberg D, Epstein RS, Kuller LH, Cauley JA: Cytokine production and bone mineral density at the lumbar spine and femoral neck in premenopausal women. Calcif Tissue Int 1998, 63: 466-470. 10.1007/s002239900559CrossRef
64.
go back to reference Cohen-Solal ME, Graulet AM, Denne MA, Gueris J, Baylink D, de Vernejoul MC: Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J Clin Endocrinol Metab 1993, 77: 1648-1653. 10.1210/jc.77.6.1648 Cohen-Solal ME, Graulet AM, Denne MA, Gueris J, Baylink D, de Vernejoul MC: Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J Clin Endocrinol Metab 1993, 77: 1648-1653. 10.1210/jc.77.6.1648
65.
go back to reference Scheidt-Nave C, Bismar H, Leidig-Bruckner G, Woitge H, Seibel MJ, Ziegler R, Pfeilschifter J: Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause. J Clin Endocrinol Metab 2001, 86: 2032-2042. 10.1210/jc.86.5.2032 Scheidt-Nave C, Bismar H, Leidig-Bruckner G, Woitge H, Seibel MJ, Ziegler R, Pfeilschifter J: Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause. J Clin Endocrinol Metab 2001, 86: 2032-2042. 10.1210/jc.86.5.2032
66.
go back to reference Kawaguchi H, Pilbeam CC, Harrison JR, Raisz LG: The role of prostaglandins in the regulation of bone metabolism. Clin Orthop Relat Res 1995, 313: 36-46. Kawaguchi H, Pilbeam CC, Harrison JR, Raisz LG: The role of prostaglandins in the regulation of bone metabolism. Clin Orthop Relat Res 1995, 313: 36-46.
67.
go back to reference Kruger MC, Coetzer H, De Winter R, Gericke G, van Papendorp DH: Calcium, gamma-linolenic acid and eicosapentaenoic acid supplementation in senile osteoporosis. Aging 1998, 10: 385-394. Kruger MC, Coetzer H, De Winter R, Gericke G, van Papendorp DH: Calcium, gamma-linolenic acid and eicosapentaenoic acid supplementation in senile osteoporosis. Aging 1998, 10: 385-394.
68.
go back to reference Kruger MC, Schollum LM: Is docosahexaenoic acid more effective than eicosapentaenoic acid for increasing calcium bioavailability? Prostaglandins Leukot Essent Fatty Acids 2005, 73: 327-334. 10.1016/j.plefa.2005.08.001CrossRef Kruger MC, Schollum LM: Is docosahexaenoic acid more effective than eicosapentaenoic acid for increasing calcium bioavailability? Prostaglandins Leukot Essent Fatty Acids 2005, 73: 327-334. 10.1016/j.plefa.2005.08.001CrossRef
69.
go back to reference Weiler HA, Fitzpatrick-Wong SC: Modulation of essential (N-6):(N-3) fatty acid ratios alters fatty acid status but not bone mass in piglets. J Nutr 2002, 132: 2667-2672. Weiler HA, Fitzpatrick-Wong SC: Modulation of essential (N-6):(N-3) fatty acid ratios alters fatty acid status but not bone mass in piglets. J Nutr 2002, 132: 2667-2672.
70.
go back to reference Parhami F: Possible role of oxidized lipids in osteoporosis: could hyperlipidemia be a risk factor? Prostaglandins Leukot Essent Fatty Acids 2003, 68: 373-378. 10.1016/S0952-3278(03)00061-9CrossRef Parhami F: Possible role of oxidized lipids in osteoporosis: could hyperlipidemia be a risk factor? Prostaglandins Leukot Essent Fatty Acids 2003, 68: 373-378. 10.1016/S0952-3278(03)00061-9CrossRef
71.
go back to reference Raisz LG, Alander CB, Simmons HA: Effects of prostaglandin E 3 and eicosapentaenoic acid on rat bone in organ culture. Prostaglandins 1989, 37: 615-625. 10.1016/0090-6980(89)90076-2CrossRef Raisz LG, Alander CB, Simmons HA: Effects of prostaglandin E 3 and eicosapentaenoic acid on rat bone in organ culture. Prostaglandins 1989, 37: 615-625. 10.1016/0090-6980(89)90076-2CrossRef
72.
go back to reference Romas G, Martin TJ: Cytokines in the pathogenesis of osteoporosis. Osteoporos Int 1997, 7: 47-53. 10.1007/BF03194342CrossRef Romas G, Martin TJ: Cytokines in the pathogenesis of osteoporosis. Osteoporos Int 1997, 7: 47-53. 10.1007/BF03194342CrossRef
73.
go back to reference Abrahamsan B, Bonnevie NV, Ebbesen EN: Cytokines and bone loss in a five year longitudinal study. J Bone and Mineral Research 2000, 15: 1545-1554. 10.1359/jbmr.2000.15.8.1545CrossRef Abrahamsan B, Bonnevie NV, Ebbesen EN: Cytokines and bone loss in a five year longitudinal study. J Bone and Mineral Research 2000, 15: 1545-1554. 10.1359/jbmr.2000.15.8.1545CrossRef
Metadata
Title
Long-term aerobic exercise and omega-3 supplementation modulate osteoporosis through inflammatory mechanisms in post-menopausal women: a randomized, repeated measures study
Authors
Bakhtyar Tartibian
Behzad Hajizadeh Maleki
Jill Kanaley
Karim Sadeghi
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Nutrition & Metabolism / Issue 1/2011
Electronic ISSN: 1743-7075
DOI
https://doi.org/10.1186/1743-7075-8-71

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