Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: A randomized, controlled trial

Journal of Bone and Mineral Research

Volumn 26, Issue 6, 2011, Pages 1339-1348

  Sukumar, Deeptha ^a   Ambia Sobhan, Hasina ^a   Zurfluh, Robert ^a   Schlussel, Yvette ^a   Stahl, Theodore J ^b   Gordon, Chris L ^c   Shapses, Sue A ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

Cortical Bone; Diet; Hormones; Insulin Like Growth Factor 1; Obesity; Protein; Trabecular Bone; Weight Loss

Indexed keywords

25 HYDROXYVITAMIN D; CALCIUM; DEOXYPYRIDINOLINE; ESTRADIOL; FAT; PARATHYROID HORMONE; PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C;

ADULT; AGED; ARTICLE; BODY MASS; BODY WEIGHT; BONE DENSITY; BONE TURNOVER; CALCIUM INTAKE; CALORIC RESTRICTION; CLINICAL ARTICLE; CONTROLLED STUDY; FAT INTAKE; FEMALE; GEOMETRY; HIP; HUMAN; LUMBAR SPINE; OSTEOLYSIS; POSTMENOPAUSE; PROTEIN DIET; PROTEIN INTAKE; RADIUS; RANDOMIZED CONTROLLED TRIAL; TIBIA; TRABECULAR BONE; WEIGHT REDUCTION;

AGED; BODY COMPOSITION; BODY WEIGHT; BONE AND BONES; BONE DENSITY; BONE REMODELING; CALORIC RESTRICTION; DIETARY PROTEINS; FEMALE; HORMONES; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR I; MIDDLE AGED; PARATHYROID HORMONE; VITAMIN D;

EID: 79958838541     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.318     Document Type: Article

References (47)

1. Conigrave AD, Brown EM, Rizzoli R,. Dietary protein and bone health: roles of amino acid-sensing receptors in the control of calcium metabolism and bone homeostasis. Annu Rev Nutr. 2008; 28: 131-155.
2. Hannan MT, Tucker KL, Dawson-Hughes B, Cupples LA, Felson DT, Kiel DP,. Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res. 2000; 15: 2504-2512.
3. Munger RG, Cerhan JR, Chiu BC,. Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am J Clin Nutr. 1999; 69: 147-152. (Pubitemid 29031265)
4. Schurch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P, Bonjour JP,. Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture: a randomized, double-blind, placebo-controlled trial. Ann Intern Med. 1998; 128: 801-809. (Pubitemid 28267712)
5. Abelow BJ, Holford TR, Insogna KL,. Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calcif Tissue Int. 1992; 50: 14-18.
6. Feskanich D, Willett WC, Stampfer MJ, Colditz GA,. Protein consumption and bone fractures in women. Am J Epidemiol. 1996; 143: 472-479. (Pubitemid 26085077)
7. Sahni S, Cupples LA, McLean R, et al. Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham Offspring Cohort. J Bone Miner Res. 2010; 25: 2770-2776.
8. Dawson-Hughes B, Harris SS,. Calcium intake influences the association of protein intake with rates of bone loss in elderly men and women. Am J Clin Nutr. 2002; 75: 773-779. (Pubitemid 34250693)
9. Shapses SA, Riedt CS,. Bone, body weight, and weight reduction: what are the concerns? J Nutr. 2006; 136: 1453-1456. (Pubitemid 43765343)
10. Jensen LB, Kollerup G, Quaade F, Sorensen OH,. Bone minerals changes in obese women during a moderate weight loss with and without calcium supplementation. J Bone Miner Res. 2001; 16: 141-147. (Pubitemid 32046199)
11. Cifuentes M, Riedt CS, Brolin RE, Field MP, Sherrell RM, Shapses SA,. Weight loss and calcium intake influence calcium absorption in overweight postmenopausal women. Am J Clin Nutr. 2004; 80: 123-130. (Pubitemid 41115565)
12. Villareal DT, Fontana L, Weiss EP, et al. Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med. 2006; 166: 2502-2510. (Pubitemid 44913236)
13. Oster MH, Fielder PJ, Levin N, Cronin MJ,. Adaptation of the growth hormone and insulin-like growth factor-I axis to chronic and severe calorie or protein malnutrition. J Clin Invest. 1995; 95: 2258-2265.
14. Shapses SA, Sukumar D,. Protein intake during weight loss: Effects on bone. In:, Burckhardt P, Dawson-Hughes B, Weaver C, eds. Nutritional Influences on Bone Health. London: Springer; 2010; 27-33.
15. Thorpe MP, Jacobson EH, Layman DK, He X, Kris-Etherton PM, Evans EM,. A diet high in protein, dairy, and calcium attenuates bone loss over twelve months of weight loss and maintenance relative to a conventional high-carbohydrate diet in adults. J Nutr. 2008; 138: 1096-1100. (Pubitemid 351769135)
16. Skov AR, Haulrik N, Toubro S, Molgaard C, Astrup A,. Effect of protein intake on bone mineralization during weight loss: a 6-month trial. Obes Res. 2002; 10: 432-438. (Pubitemid 135686634)
17. Campbell WW, Tang M,. Protein intake, weight loss, and bone mineral density in postmenopausal women. J Gerontol A Biol Sci Med Sci. 2010; 65: 1115-1122.
18. Lewiecki EM, Gordon CM, Baim S, et al. International Society for Clinical Densitometry 2007 Adult and Pediatric Official Positions. Bone. 2008; 43: 1115-1121.
19. Sukumar D, Schlussel Y, Riedt CS, Gordon C, Stahl T, Shapses SA,. Obesity alters cortical and trabecular bone density and geometry in women. Osteoporos Int. 2011; 22: 635-645.
20. Westerterp-Plantenga MS, Nieuwenhuizen A, Tome D, Soenen S, Westerterp KR,. Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr. 2009; 29: 21-41.
21. Sacks FM, Bray GA, Carey VJ, et al. Comparison of weight-loss diets with different compositions of fat, protein, and carbohydrates. N Engl J Med. 2009; 360: 859-873.
22. Clifton PM, Keogh JB, Noakes M,. Long-term effects of a high-protein weight-loss diet. Am J Clin Nutr. 2008; 87: 23-29.
23. Holmes MD, Pollak MN, Willett WC, Hankinson SE,. Dietary correlates of plasma insulin-like growth factor I and insulin-like growth factor binding protein 3 concentrations. Cancer Epidemiol Biomarkers Prev. 2002; 11: 852-861. (Pubitemid 35014888)
24. Price JS, Oyajobi BO, Oreffo RO, Russell RG,. Cells cultured from the growing tip of red deer antler express alkaline phosphatase and proliferate in response to insulin-like growth factor-I. J Endocrinol. 1994; 143: R9-16. (Pubitemid 24347774)
25. Kerstetter JE, O'Brien KO, Caseria DM, Wall DE, Insogna KL,. The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab. 2005; 90: 26-31. (Pubitemid 40116629)
26. Roughead ZK, Hunt JR, Johnson LK, Badger TM, Lykken GI,. Controlled substitution of soy protein for meat protein: effects on calcium retention, bone, and cardiovascular health indices in postmenopausal women. J Clin Endocrinol Metab. 2005; 90: 181-189. (Pubitemid 40116654)
27. Hunt JR, Johnson LK, Fariba Roughead ZK,. Dietary protein and calcium interact to influence calcium retention: a controlled feeding study. Am J Clin Nutr. 2009; 89: 1357-1365.
28. Ricci TA, Heymsfield SB, Pierson RN Jr, Stahl T, Chowdhury HA, Shapses SA,. Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J Clin Nutr. 2001; 73: 347-352. (Pubitemid 32109866)
29. Riedt CS, Cifuentes M, Stahl T, Chowdhury HA, Schlussel Y, Shapses SA,. Overweight postmenopausal women lose bone with moderate weight reduction and 1g/day calcium intake. J Bone Miner Res. 2005; 20: 455-463. (Pubitemid 40293494)
30. Ammann P, Bourrin S, Bonjour JP, Meyer JM, Rizzoli R,. Protein undernutrition-induced bone loss is associated with decreased IGF-I levels and estrogen deficiency. J Bone Miner Res. 2000; 15: 683-690. (Pubitemid 30174022)
31. Noakes M, Keogh JB, Foster PR, Clifton PM,. Effect of an energy-restricted, high-protein, low-fat diet relative to a conventional high-carbohydrate, low-fat diet on weight loss, body composition, nutritional status, and markers of cardiovascular health in obese women. Am J Clin Nutr. 2005; 81: 1298-1306. (Pubitemid 41710230)
32. Bowen J, Noakes M, Clifton PM,. A high dairy protein, high-calcium diet minimizes bone turnover in overweight adults during weight loss. J Nutr. 2004; 134: 568-573. (Pubitemid 38298497)
33. Dawson-Hughes B, Harris SS, Krall EA, Dallal GE,. Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. N Engl J Med. 1997; 337: 670-676. (Pubitemid 27375473)
34. Yakar S, Rosen CJ, Beamer WG, et al. Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest. 2002; 110: 771-781.
35. Heaney RP, McCarron DA, Dawson-Hughes B, et al. Dietary changes favorably affect bone remodeling in older adults. J Am Diet Assoc. 1999; 99: 1228-1233. (Pubitemid 29480614)
36. Khalil DA, Lucas EA, Juma S, Smith BJ, Payton ME, Arjmandi BH,. Soy protein supplementation increases serum insulin-like growth factor-I in young and old men but does not affect markers of bone metabolism. J Nutr. 2002; 132: 2605-2608. (Pubitemid 35013242)
37. Dawson-Hughes B, Harris SS, Rasmussen H, Song L, Dallal GE,. Effect of dietary protein supplements on calcium excretion in healthy older men and women. J Clin Endocrinol Metab. 2004; 89: 1169-1173. (Pubitemid 38368407)
38. Roughead ZK, Johnson LK, Lykken GI, Hunt JR,. Controlled high meat diets do not affect calcium retention or indices of bone status in healthy postmenopausal women. J Nutr. 2003; 133: 1020-1026. (Pubitemid 36407119)
39. Grinspoon SK, Baum HB, Peterson S, Klibanski A,. Effects of rhIGF-I administration on bone turnover during short-term fasting. J Clin Invest. 1995; 96: 900-906.
40. Sugimoto T, Nishiyama K, Kuribayashi F, Chihara K,. Serum levels of insulin-like growth factor (IGF) I, IGF-binding protein (IGFBP)-2, and IGFBP-3 in osteoporotic patients with and without spinal fractures. J Bone Miner Res. 1997; 12: 1272-1279. (Pubitemid 27334974)
41. Ghiron LJ, Thompson JL, Holloway L, et al. Effects of recombinant insulin-like growth factor-I and growth hormone on bone turnover in elderly women. J Bone Miner Res. 1995; 10: 1844-1852.
42. O'Dea JP, Wieland RG, Hallberg MC, Llerena LA, Zorn EM, Genuth SM,. Effect of dietery weight loss on sex steroid binding sex steroids, and gonadotropins in obese postmenopausal women. J Lab Clin Med. 1979; 93: 1004-1008. (Pubitemid 10217495)
43. Ettinger B, Ensrud KE, Wallace R, et al. Effects of ultralow-dose transdermal estradiol on bone mineral density: a randomized clinical trial. Obstet Gynecol. 2004; 104: 443-451. (Pubitemid 40458828)
44. Prestwood KM, Kenny AM, Kleppinger A, Kulldorff M,. Ultralow-dose micronized 17beta-estradiol and bone density and bone metabolism in older women: a randomized controlled trial. JAMA. 2003; 290: 1042-1048. (Pubitemid 37430444)
45. Tzotzas T, Papadopoulou FG, Tziomalos K, et al. Rising serum 25-hydroxy-vitamin D levels after weight loss in obese women correlate with improvement in insulin resistance. J Clin Endocrinol Metab. 2010; 95: 4251-4257.
46. Wortsman J, Matsuoka LY, Chen TC, Lu Z, Holick MF,. Decreased bioavailability of vitamin D in obesity. Am J Clin Nutr. 2000; 72: 690-693. (Pubitemid 30667088)
47. Bolotin HH,. A new perspective on the causal influence of soft tissue composition on DXA-measured in vivo bone mineral density. J Bone Miner Res. 1998; 13: 1739-1746. (Pubitemid 28492004)