Reduced bone mineral density is not associated with significantly reduced bone quality in men and women practicing long-term calorie restriction with adequate nutrition

Aging Cell

Volumn 10, Issue 1, 2011, Pages 96-102

  Villareal, Dennis T ^a,b   Kotyk, John J ^c   Armamento Villareal, Reina C ^a,b   Kenguva, Venkata ^a   Seaman, Pamela ^d   Shahar, Allon ^d   Wald, Michael J ^e   Kleerekoper, Michael ^e   Fontana, Luigi ^a,f  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MicroMRI Inc   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Bone mineral density; Bone quality; Bone turnover; Calorie restriction; High resolution magnetic resonance imaging; Trabecular bone microarchitecture

Indexed keywords

ALKALINE PHOSPHATASE; C REACTIVE PROTEIN; CARBOXY TERMINAL TELOPEPTIDE;

ADULT; ARTICLE; BONE DENSITY; BONE EROSION; BONE TURNOVER; CALORIC RESTRICTION; CONTROLLED STUDY; DIETARY INTAKE; FEMALE; HIP; HUMAN; HUMAN EXPERIMENT; LUMBAR SPINE; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RADIUS; SEDENTARY LIFESTYLE; TRABECULAR BONE;

ALKALINE PHOSPHATASE; BODY COMPOSITION; BODY MASS INDEX; BONE AND BONES; BONE DENSITY; C-REACTIVE PROTEIN; CALORIC RESTRICTION; COLLAGEN TYPE I; CROSS-SECTIONAL STUDIES; FEMALE; FRACTURES, BONE; HIP; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NUTRITIONAL REQUIREMENTS; PEPTIDES; RISK FACTORS; TIME;

RODENTIA;

EID: 78651342474     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00643.x     Document Type: Article

References (52)

1. Aaron JE, Shore PA, Shore RC, Beneton M, Kanis JA (2000) Trabecular architecture in women and men of similar bone mass with and without vertebral fracture: II. Three-dimensional histology. Bone 27, 277-282.
2. Aerssens J, Boonen S, Lowet G, Dequeker J (1998) Interspecies differences in bone composition, density, and quality: potential implications for in vivo bone research. Endocrinology 139, 663-670.
3. Anderson RM, Shanmuganayagam D, Weindruch R (2009) Caloric restriction and aging: studies in mice and monkeys. Toxicol. Pathol. 37, 47-51.
4. Benito M, Vasilic B, Wehrli FW, Bunker B, Wald M, Gomberg B, Wright AC, Zemel B, Cucchiara A, Snyder PJ (2005) Effect of testosterone replacement on trabecular architecture in hypogonadal men. J. Bone Miner. Res. 20, 1785-1791.
5. Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR (1986) Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319, 516-518.
6. Bjarnason NH, Sarkar S, Duong T, Mitlak B, Delmas PD, Christiansen C (2001) Six and twelve month changes in bone turnover are related to reduction in vertebral fracture risk during 3 years of raloxifene treatment in postmenopausal osteoporosis. Osteoporos. Int. 12, 922-930.
7. Blaum CS, Xue QL, Michelon E, Semba RD, Fried LP (2005) The association between obesity and the frailty syndrome in older women: the women's health and aging studies. J. Am. Geriatr. Soc. 53, 927-934.
8. Cesari M, Penninx BW, Newman AB, Kritchevsky SB, Nicklas BJ, Sutton-Tyrrell K, Rubin SM, Ding J, Simonsick EM, Harris TB, Pahor M (2003) Inflammatory markers and onset of cardiovascular events: results from the Health ABC study. Circulation 108, 2317-2322.
9. Cummings SR, Karpf DB, Harris F, Genant HK, Ensrud K, LaCroix AZ, Black DM (2002) Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs. Am. J. Med. 112, 281-289.
10. Dempster DW (2003) Bone microarchitecture and strength. Osteoporos. Int. 14(Suppl. 5), S54-S56.
11. Ding C, Parameswaran V, Udayan R, Burgess J, Jones G (2008) Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J. Clin. Endocrinol. Metab. 93, 1952-1958.
12. Fontana L, Klein S (2007) Aging, adiposity, and calorie restriction. JAMA 297, 986-994.
13. Fontana L, Weiss EP, Villareal DT, Klein S, Holloszy JO (2008) Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Aging Cell 7, 681-687.
14. Gomberg BR, Wehrli FW, Vasilic B, Weening RH, Saha PK, Song HK, Wright AC (2004) Reproducibility and error sources of micro-MRI-based trabecular bone structural parameters of the distal radius and tibia. Bone 35, 266-276.
15. Greenspan SL, Perera S, Recker R, Wagner JM, Greeley P, Gomberg BR, Seaman P, Kleerekoper M (2010) Changes in trabecular microarchitecture in postmenopausal women on bisphosphonate therapy. Bone 46, 1006-1010.
16. Hamrick MW, Ding KH, Ponnala S, Ferrari SL, Isales CM (2008) Caloric restriction decreases cortical bone mass but spares trabecular bone in the mouse skeleton: implications for the regulation of bone mass by body weight. J. Bone Miner. Res. 23, 870-878.
17. Homminga J, McCreadie BR, Ciarelli TE, Weinans H, Goldstein SA, Huiskes R (2002) Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level. Bone 30, 759-764.
18. Ilich JZ, Kerstetter JE (2000) Nutrition in bone health revisited: a story beyond calcium. J. Am. Coll. Nutr. 19, 715-737.
19. Johnell O, Oden A, De LC, Garnero P, Delmas PD, Kanis JA (2002) Biochemical indices of bone turnover and the assessment of fracture probability. Osteoporos. Int. 13, 523-526.
20. Kalu DN, Hardin RR, Cockerham R, Yu BP, Norling BK, Egan JW (1984) Lifelong food restriction prevents senile osteopenia and hyperparathyroidism in F344 rats. Mech. Aging Dev. 26, 103-112.
21. Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM (1985) The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif. Tissue Int. 37, 594-597.
22. Koh JM, Khang YH, Jung CH, Bae S, Kim DJ, Chung YE, Kim GS (2005) 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. 16, 1263-1271.
23. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, Wong T, Campagnuolo G, Moran E, Bogoch ER, Van G, Nguyen LT, Ohashi PS, Lacey DL, Fish E, Boyle WJ, Penninger JM (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402, 304-309.
24. Lambert J, Lamothe JM, Zernicke RF, Auer RN, Reimer RA (2005) Dietary restriction does not adversely affect bone geometry and mechanics in rapidly growing male wistar rats. Pediatr. Res. 57, 227-231.
25. Lamothe JM, Hepple RT, Zernicke RF (2003) Selected contribution: bone adaptation with aging and long-term caloric restriction in Fischer 344 x Brown-Norway F1-hybrid rats. J. Appl. Physiol. 95, 1739-1745.
26. Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle MF, Audran M (2000) Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J. Bone Miner. Res. 15, 13-19.
27. Ma J, Wehrli FW, Song HK (1996) Fast 3D large-angle spin-echo imaging (3D FLASE). Magn. Reson. Med. 35, 903-910.
28. McCay CM, Crowell MF, Maynard LA (1989) The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935. Nutrition 5, 155-171.
29. Muhlbauer RC, Li F (1999) Effect of vegetables on bone metabolism. Nature 401, 343-344.
30. Oelzner P, Franke S, Muller A, Hein G, Stein G (1999) Relationship between soluble markers of immune activation and bone turnover in post-menopausal women with rheumatoid arthritis. Rheumatology 38, 841-847.
31. Ravn P, Cizza G, Bjarnason NH, Thompson D, Daley M, Wasnich RD, McClung M, Hosking D, Yates AJ, Christiansen C (1999) Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women. Early Postmenopausal Intervention Cohort (EPIC) study group. J. Bone Miner. Res. 14, 1622-1627.
32. Reddy GK, Stehno-Bittel L, Hamade S, Enwemeka CS (2001) The biomechanical integrity of bone in experimental diabetes. Diabetes Res. Clin. Pract. 54, 1-8.
33. Riggs BL, Melton Iii LJ, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S (2004) Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J. Bone Miner. Res. 19, 1945-1954.
34. Ross PD, Norimatsu H, Davis JW, Yano K, Wasnich RD, Fujiwara S, Hosoda Y, Melton III LJ (1991) A comparison of hip fracture incidence among native Japanese, Japanese Americans, and American Caucasians. Am. J. Epidemiol. 133, 801-809.
35. Ross PD, Kress BC, Parson RE, Wasnich RD, Armour KA, Mizrahi IA (2000) Serum bone alkaline phosphatase and calcaneus bone density predict fractures: a prospective study. Osteoporos. Int. 11, 76-82.
36. Sarkar S, Mitlak BH, Wong M, Stock JL, Black DM, Harper KD (2002) Relationships between bone mineral density and incident vertebral fracture risk with raloxifene therapy. J. Bone Miner. Res. 17, 1-10.
37. Saville PD, Lieber CS (1969) Increases in skeletal calcium and femur cortex thickness produced by undernutrition. J. Nutr. 99, 141-144.
38. Schett G, Kiechl S, Weger S, Pederiva A, Mayr A, Petrangeli M, Oberhollenzer F, Lorenzini R, Redlich K, Axmann R, Zwerina J, Willeit J (2006) High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch. Intern. Med. 166, 2495-2501.
39. Schwartz AV (2003) Diabetes mellitus: does it affect bone? Calcif. Tissue Int. 73, 515-519.
40. Seeman E, Delmas PD (2006) Bone quality-the material and structural basis of bone strength and fragility. N. Engl. J. Med. 354, 2250-2261.
41. Silverman SL, Madison RE (1988) Decreased incidence of hip fracture in Hispanics, Asians, and blacks: California Hospital Discharge Data. Am. J. Public Health 78, 1482-1483.
42. Slemenda CW (1995) Body composition and skeletal density-mechanical loading or something more? J. Clin. Endocrinol. Metab. 80, 1761-1763.
43. Takayanagi H (2007) Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat. Rev. Immunol. 7, 292-304.
44. Talbott SM, Cifuentes M, Dunn MG, Shapses SA (2001) Energy restriction reduces bone density and biomechanical properties in aged female rats. J. Nutr. 131, 2382-2387.
45. Tatsumi S, Ito M, Asaba Y, Tsutsumi K, Ikeda K (2008) Life-long caloric restriction reveals biphasic and dimorphic effects on bone metabolism in rodents. Endocrinology 149, 634-641.
46. Theill LE, Boyle WJ, Penninger JM (2002) RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu. Rev. Immunol. 20, 795-823.
47. Verhaeghe J, Suiker AM, Einhorn TA, Geusens P, Visser WJ, Van HE, Van BR, Magitsky S, Bouillon R (1994) Brittle bones in spontaneously diabetic female rats cannot be predicted by bone mineral measurements: studies in diabetic and ovariectomized rats. J. Bone Miner. Res. 9, 1657-1667.
48. Wehrli FW (2007) Structural and functional assessment of trabecular and cortical bone by micro magnetic resonance imaging. J. Magn. Reson. Imaging 25, 390-409.
49. Wehrli FW, Hwang SN, Ma J, Song HK, Ford JC, Haddad JG (1998) Cancellous bone volume and structure in the forearm: noninvasive assessment with MR microimaging and image processing. Radiology 206, 347-357.
50. Wehrli FW, Gomberg BR, Saha PK, Song HK, Hwang SN, Snyder PJ (2001) Digital topological analysis of in vivo magnetic resonance microimages of trabecular bone reveals structural implications of osteoporosis. J. Bone Miner. Res. 16, 1520-1531.
51. Wehrli FW, Saha PK, Gomberg BR, Song HK, Snyder PJ, Benito M, Wright A, Weening R (2002) Role of magnetic resonance for assessing structure and function of trabecular bone. Top. Magn. Reson. Imaging 13, 335-355.
52. Westerbeek ZW, Hepple RT, Zernicke RF (2008) Effects of aging and caloric restriction on bone structure and mechanical properties. J. Gerontol. A Biol. Sci. Med. Sci. 63, 1131-1136.