A grape-enriched diet increases bone calcium retention and cortical bone properties in ovariectomized rats

Journal of Nutrition

Volumn 145, Issue 2, 2015, Pages 253-259

  Hohman, Emily E ^a   Weaver, Connie M ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Bone; Calcium; Grape; Osteoporosis; Rats

Indexed keywords

CALCIUM; CALCIUM 45;

ANIMAL EXPERIMENT; ARTICLE; BONE DENSITY; BONE STRENGTH; CALCIUM ABSORPTION; CALCIUM BALANCE; CALCIUM BONE LEVEL; CONTROLLED STUDY; CORTICAL BONE; CORTICAL THICKNESS (BONE); DIET; GRAPE; NONHUMAN; RAT; ANIMAL; BODY WEIGHT; BONE; FEMALE; FRUIT; METABOLISM; OVARIECTOMY; SPRAGUE DAWLEY RAT; VITIS;

RATTUS; VITACEAE;

ANIMALS; BODY WEIGHT; BONE AND BONES; BONE DENSITY; CALCIUM; DIET; FEMALE; FRUIT; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; VITIS;

EID: 84922206064     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.114.198598     Document Type: Article

References (63)

1. Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, Dawson-Hughes B. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res 2014;29:2520-6.
2. Pinkerton JV, Thomas S, Dalkin AC. Osteoporosis treatment and prevention for postmenopausal women: current and future therapeutic options. Clin Obstet Gynecol 2013;56:711-21.
3. Kothawala P, Badamgarav E, Ryu S, Miller RM, Halbert RJ. Systematic review and meta-analysis of real-world adherence to drug therapy for osteoporosis. Mayo Clin Proc 2007;82:1493-501.
4. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321-33.
5. Shane E, Burr D, Abrhamsen B, Adler RA, Brown TD, Cheung AM, Cosman F, Curtis JR, Dell R, Dempster DW, et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 2014;29:1-23.
6. Reid IR, Cornish J. Epidemiology and pathogenesis of osteonecrosis of the jaw. Nat Rev Rheumatol. 2012;8:90-6.
7. Cipriani C, Irani D, Bilezikian JP. Safety of osteoanabolic therapy: a decade of experience. J Bone Miner Res 2012;27:2419-28.
8. Vislocky LM, Fernandez ML. Biomedical effects of grape products. Nutr Rev 2010;68:656-70.
9. Xu Y, Simon JE, Welch C, Wightman JD, Ferruzzi MG, Ho L, Pasinetti GM, Wu Q. Survey of polyphenol constituents in grapes and grapederived products. J Agric Food Chem 2011;59:10586-93.
10. Cantos E, Espín JC, Tomás-Barberán FA. Varietal differences among polyphenol profiles of seven table grape cultivars studied by LC-DADMS- MS. J Agric Food Chem 2002;50:5691-6.
11. Yin J, Winzenberg T, Quinn S, Giles G, Jones G. Beverage-specific alcohol intake and bone loss in older men and women: a longitudinal study. Eur J Clin Nutr 2011;65:526-32.
12. Welch A, MacGregor A, Jennings A, Fairweather-Tait S, Spector T, Cassidy A. Habitual flavonoid intakes are positively associated with bone mineral density in women. J Bone Miner Res 2012;27:1872-8.
13. Hardcastle AC, Aucott L, Reid DM, MacDonald HM. Associations between dietary flavonoid intake and bone health in a Scottish population. J Bone Miner Res 2011;26:941-7.
14. Siddiqui JA, Sharan K, Swarnkar G, Rawat P, Kumar M, Manickavasagan L, Maurya R, Pierroz D, Chattopadhyay N. Quercetin-6-C-b-Dglucopyranoside isolated from Ulmus wallichiana planchon is more potent than quercetin in inhibiting osteoclastogenesis and mitigating ovariectomy-induced bone loss in rats. Menopause 2011;18:198-207.
15. Trivedi R, Kumar S, Kumar A, Siddiqui JA, Swarnkar G, Gupta V, Kendurker A, Dwivedi AK, Romero JR, Chattopadhyay N. Kaempferol has osteogenic effect in ovariectomized adult Sprague-Dawley rats. Mol Cell Endocrinol 2008;289:85-93.
16. Liu ZP, Li WX, Yu B, Huang J, Sun J, Huo JS, Liu CX. Effects of transresveratrol from Polygonum cuspidatum on bone loss using the ovariectomized rat model. J Med Food 2005;8:14-9.
17. Shen CL, Wang P, Guerrieri J, Yeh JK, Wang JS. Protective effect of green tea polyphenols on bone loss in middle-aged female rats. Osteoporos Int 2008;19:979-90.
18. Yahara N, Tofani I, Maki K, Kojima K, Kimura M. Mechanical assessment of effects of grape seed proanthocyanidins extract on tibial bone diaphysis in rats. J Musculoskelet Neuronal Interact 2005;5:162-9.
19. Mühlbauer RC, Lozano A, Reinli A, Wetli H. Various selected vegetables, fruits, mushrooms and red wine residue inhibit bone resorption in rats. J Nutr 2003;133:3592-7.
20. Pawlowski JW, Martin BR, McCabe GP, Ferruzzi MG, Weaver CM. Polyphenolic-rich extracts of plum, soy, and resveratrol improve bone calcium retention in ovariectomized Sprague Dawley rats. J Agric Food Chem 2014;62:6108-17.
21. Reeves PG, Nielsen FH, Fahey GC. 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 1993;123:1939-51.
22. Zafar TA, Weaver CM, Zhao Y, Martin BR, Wastney ME. Nondigestible oligosaccharides increase calcium absorption and suppress bone resorption in ovariectomized rats. J Nutr 2004;134:399-402.
23. Cai J, Zhang Q, Wastney ME, Weaver CM. Calcium bioavailability and kinetics of calcium ascorbate and calcium acetate in rats. Exp Biol Med (Maywood) 2004;229:40.
24. Hohman EE, Martin BR, Lachcik PJ, Gordon DT, Fleet JC, Weaver CM. Bioavailability and efficacy of vitamin D2 from UV-irradiated yeast in growing, vitamin D-deficient rats. J Agric Food Chem 2011;59:2341-6.
25. Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone 1993;14:595-608.
26. Rendina E, Hembree KD, Davis MR, Marlow D, Clarke SL, Halloran BP, Lucas EA, Smith BJ. Dried plum's unique capacity to reverse bone loss and alter bone metabolism in postmenopausal osteoporosis model. PLoS ONE 2013;8:e60569.
27. Legette LL, Lee WH, Martin BR, Story JA, Arabshahi A, Barnes S, Weaver CM. Genistein, a phytoestrogen, improves total cholesterol, and Synergy, a prebiotic, improved calcium utilization but there were no synergistic effects. Menopause 2011;18:923-31.
28. Ariefdjohan MW, Martin BR, Lachcik PJ, Weaver CM. Acute and chronic effects of honey and its carbohydrate constituents on calcium absorption in rats. J Agric Food Chem 2008;56:2649-54.
29. Zhao Y, Martin BR, Wastney ME, Schollum L, Weaver CM. Acute versus chronic effects of whey proteins on calcium absorption in growing rats. Exp Biol Med (Maywood) 2005;230:536-42.
30. Ohta A, Ohtsuki M, Baba S, Adachi T, Sakata T, Sakaguchi E. Calcium and magnesium absorption from the colon and rectum are increased in rats fed fructooligosaccharides. J Nutr 1995;125:2417-24.
31. Barger-Lux MJ, Heaney RP, Recker RR. Time course of calcium absorption in humans: evidence for a colonic compartment. Calcif Tissue Int 1989;44:308-11.
32. Danielsen CC, Mosekilde L, Svenstrup B. Cortical bone mass, composition, and mechanical properties in female rats in relation to age, longterm ovariectomy, and estrogen susbstitution. Calcif Tissue Int 1993; 52:26-33.
33. Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas DP. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 2006;21:1856-63.
34. Perilli E, Le V, Ma B, Salmon P, Reynolds K, Fazzalari NL. Detecting early changes using in vivo micro-CT in ovariectomized, zoledronic acidtreated, and sham-operated rats. Osteoporos Int 2010;21:1371-82.
35. Weaver C, Cheong J, Jackson G, Elmore D, McCabe G, Martin B. 3H-tetracycline as a proxy for 41Ca for measuring perturbations of bone resorption. Nucl Instrum Methods Phys Res B 2007;259:790-5.
36. Dawson-Hughes B, Dallal GE, Krall EA, Sadowski L, Sahyoun N, Tannenbaum S. A controlled trial of the effect of calcium supplementation on bone density in postmenopausal women. N Engl J Med 1990;323:878-83.
37. Klinge CM, Risinger KE, Watts MB, Beck V, Eder R, Jungbauer A. Estrogenic activity in white and red wine extracts. J Agric Food Chem 2003;51:1850-7.
38. Bowers JL, Tyulmenkov VV, Jernigan SC, Klinge CM. Resveratrol acts as a mixed agonist/antagonist for estrogen receptors a and b. Endocrinology 2000;141:3657-67.
39. Resende FA, de Oliveira APS, de Camargo MS, Vilegas W, Varanda EA. Evaluation of estrogenic potential of flavonoids using a recombinant yeast strain and MCF7/BUS cell proliferation assay. PLoS ONE 2013;8: e74881.
40. Tang X, Zhu X, Liu S, Nicholson RC, Ni X. Phytoestrogens induce differential estrogen receptor b-mediated responses in transfected MG-63 cells. Endocrine 2008;34:29-35.
41. Schmitt E, Stopper H. Estrogenic activity of naturally occurring anthocyanidins. Nutr Cancer 2001;41:145-9.
42. Rassi CM, Lieberherr M, Chaumaz G, Pointillart A, Cournot G. Modulation of osteoclastogenesis in porcine bone marrow cultures by quercetin and rutin. Cell Tissue Res 2005;319:383-93.
43. He X, Andersson G, Lindgren U, Li Y. Resveratrol prevents RANKLinduced osteoclast differentiation of murine osteoclast progenitor RAW 264.7 through inhibition of ROS production. Biochem Biophys Res Commun 2010;401:356-62.
44. Tseng PC, Hou SM, Chen RJ, Peng HW, Hsieh CF, Kuo ML, Yen ML. Resveratrol promotes osteogenesis of human mesenchymal stem cells by upregulating RUNX2 gene expression via the SIRT1/FOXO3A axis. J Bone Miner Res 2011;26:2552-63.
45. Pang JL, Ricupero DA, Huang S, Fatma N, Singh DP, Romero JR, Chattopadhyay N. Differential activity of kaempferol and quercetin in attenuating tumor necrosis factor receptor family signaling in bone cells. Biochem Pharmacol 2006;71:818-26.
46. Srivastava S, Bankar R, Roy P. Assessment of the role of flavonoids for inducing osteoblast differentiation in isolated bone marrow derived mesenchymal stem cells. Phytomedicine 2013;20:683-90.
47. Miyake M, Arai N, Ushio S, Iwaki K, Ikeda M, Kurimoto M. Promoting effect of kaempferol on the differentiation and mineralization of murine pre-osteoblastic cell line MC3T3-E1. Biosci Biotechnol Biochem 2003; 67:1199-205.
48. Park JS, Park MK, Oh HJ, Woo YJ, Lim MA, Lee JH, Ju JH, Jung YO, Lee ZH, Park SH, et al. Grape-seed proanthocyanidin extract as suppressors of bone destruction in inflammatory autoimmune arthritis. PLoS ONE 2012;7:e51377.
49. Choi EM, Hwang JK. Effects of (+)-catechin on the function of osteoblastic cells. Biol Pharm Bull 2003;26:523-6.
50. Mundy GR. Osteoporosis and inflammation. Nutr Rev 2007;65: S147-51.
51. Richard N, Porath D, Radspieler A, Schwager J. Effects of resveratrol, piceatannol, tri-acetoxystilbene, and genistein on the inflammatory response of human peripheral blood leukocytes. Mol Nutr Food Res 2005;49:431-42.
52. Wang J, Mazza G. Inhibitory effects of anthocyanins and other phenolic compounds on nitric oxide production in LPS/IFN-g-activated RAW 264.7 macrophages. J Agric Food Chem 2002;50:850-7.
53. Terra X, Valls J, Vitrac X, Mérrillon JM, Arola L, Ardévol A, Bladé C, Fernández-Larrea J, Pujadas G, Salvadó J, et al. Grape-seed proanthocyanidins act as antiinflammatory agents in endotoxin stimulated RAW 264.7 macrophages by inhibiting NFkB signaling pathway. J Agric Food Chem 2007;55:4357-65.
54. Zhu K, Devine A, Prince RL. The effects of high potassium consumption on bone mineral density in a prospective cohort study of elderly postmenopausal women. Osteoporos Int 2009;20:335-40.
55. Moseley KF, Weaver CM, Appel L, Sebastian A, Sellmeyer DE. Potassium citrate supplementation results in sustained improvement in calcium balance in older men and women. J Bone Miner Res 2013; 28:497-504.
56. Jehle S, Hulter HN, Krapf R. Effect of potassium citrate on bone density, microarchitecture, and fracture risk in healthy older adults without osteoporosis: a randomized controlled trial. J Clin Endocrinol Metab 2013;98:207-17.
57. Dai Z, Wang R, Ang LW, Low YL, Yuan JM, Koh WP. Protective effects of dietary carotenoids on risk of hip fracture in men: the Singapore Chinese Health Study. J Bone Miner Res 2014;29:408-17.
58. Sahni S, Hannan MT, Blumberg J, Cupples LA, Kiel DP, Tucker KL. Inverse association of carotenoid intakes with 4-y change in bone mineral density in elderly men and women: the Framingham Osteoporosis Study. Am J Clin Nutr 2009;89:416-24.
59. Ryder KM, Shorr RI, Bush AJ, Kritchevsky SB, Harris T, Stone K, Cauley J, Tylavsky FA.Magnesium intake from food and supplements is associated with bone mineral density in healthy older white subjects. J Am Geriatr Soc 2005;53:1875-80.
60. Toba Y, Kajita Y, Masuyama R, Takada Y, Suzuki K, Aoe S. Dietary magnesium supplementation affects bone metabolism and dynamic strength in ovariectomized rats. J Nutr 2000;130:216-20.
61. Rico H, Roca-Botran C, Hernandez ER, Seco C, Paez E, Valencia MJ, Villa LF. The effect of supplemental copper on osteopenia induced by ovariectomy in rats. Menopause 2000;7:413-6.
62. Halloran BP, Wronski TJ, VonHerzen DC, Chu V, Xia X, Pingel JE, Williams AA, Smith BJ. Dietary dried plum increases bone mass in adult and aged male mice. J Nutr 2010;140:1781-7.
63. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008;22:659-61.