![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
School of Allied Health, University of Connecticut, Storrs, CT 06269-2101,
*
Johns Hopkins Bloomberg School of Public Health, Center for Human Nutrition, Baltimore, MD 21218 and
Yale University School of Internal Medicine, New Haven, CT 06520-8020
3To whom correspondence should be addressed. E-mail: Jane.Kerstetter{at}uconn.edu
 |
ABSTRACT |
|---|
 TOP ABSTRACT Dietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
KEY WORDS: • dietary protein • urinary calcium • calcium absorption • parathyroid hormone • bone
Almost 10 million Americans have been diagnosed with osteoporosis and 34 million have osteopenia (1 ). The health problems that accompany low bone mass are reaching near epidemic proportions in the United States and worldwide. There is little doubt that dietary calcium and vitamin D are critical nutrients for both accruing and maintaining skeletal mass. Compared to calcium and vitamin D, much less is known about how other nutrients, such as dietary protein, affect bone. A long-standing hypothesis was that a high protein diet was detrimental to bone because it generated a high endogenous acid load that would require buffering from bone, thereby increasing resorption (2 ). However, recent nutrition intervention trials and epidemiological data suggest that high protein diet–induced hypercalciuria is attributable, for the most part, to increased intestinal calcium absorption, leaving uncertain the effect that a high protein diet has on the skeleton. In contrast, low protein diets decrease intestinal calcium absorption (see below) and in the majority of recent epidemiological studies, are associated with reduced bone mass. This review summarizes our current understanding of the effects of a protein-restricted diet on calcium and bone homeostasis.
|
Dietary protein and calcium in the United States |
|---|
|
TOPABSTRACTDietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
|
|
|
The traditional view |
|---|
|
TOPABSTRACTDietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
 |
where urine Ca is expressed as mmol/d and dietary protein is g/d, slope = 3.208E-02 and y-intercept is 1.501. These data clearly establish that dietary protein is an important regulator of urinary calcium excretion, at least as important as dietary calcium (11 ,31 ).
|
The above "bone hypothesis" was further supported by the observation that dietary protein reportedly does not affect intestinal Ca absorption. Most human balance studies report no difference in Ca absorption when dietary protein is altered (7 –12 ,15 ,18 ,60 ), although there are a few exceptions (6 ,16 ,61 ).
However, studies conducted over the past 8 y in our laboratory call the traditional high protein bone hypothesis to question. We have found that a high protein diet induces hypercalciuria primarily because it increases intestinal Ca absorption. Second, a low protein diet acutely reduces intestinal Ca absorption, resulting in an abrupt rise in serum parathyroid hormone. Finally, emerging epidemiological data from our group and others suggest that the long-term consequences of these changes in intestinal handling of Ca may adversely affect skeletal homeostasis. In this review, we summarize the most recent nutrition intervention trials and the epidemiological studies that suggest a need to revisit our traditional thinking about how dietary protein affects bone.
|
The acute impact of low protein diets |
|---|
|
TOPABSTRACTDietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
In 1997 we reported the short-term effect of three levels of dietary protein [low (0.7 g/kg), medium (1.0 g/kg) and high (2.1 g/kg)] on calcium metabolism in 16 healthy women (age 26.7 ± 1.3 y) (22 ). The study consisted of three interventions, each of which included 2 wk of a well-balanced adjustment diet (moderate calcium, sodium and protein) followed by an experimental period of 4 d (or 14 d in 7 subjects). During the experimental period, all diets contained 40 mmol calcium and 100 mEq sodium. Alcohol was not permitted and caffeinated beverages were limited to one a day. All foods on the experimental diet were weighed to within 0.1 g in the General Clinical Research Center kitchen and subjects consumed all of the experimental diet. All diets were consumed in random order by all subjects, thus permitting the use of a repeated-measures ANOVA for the statistical analyses.
As expected, the rise in urinary calcium excretion mirrored the rise in dietary protein intake at 4 d. Mean 24-h urinary calcium excretion during the three diets was 2.7 ± 0.3 (low protein), 3.2 ± 0.3 (medium protein) and 4.9 ± 0.5 (high protein) mmol/d. The most surprising finding in the first study was that by d 4 of the low protein diet, striking elevations in serum parathyroid hormone (PTH) and circulating concentrations of 1,25(OH)2vitamin D (calcitriol) developed in all subjects (Fig. 2 ). In fact, concentrations of these calcitropic hormones, in most cases, exceeded the upper limits of normal. Serum PTH was increased 1.5- to 2.4-fold by d 4 and 1.6- to 2.7-fold by d 14 over values seen in subjects consuming a moderate (1.0 g/kg) protein intake. The rise in PTH was accompanied by significant increases in both serum calcitriol and nephrogenous cyclic AMP excretion (NcAMP, a sensitive and specific indicator of PTH bioactivity). Thus, healthy young women abruptly developed secondary hyperparathyroidism within 4 d of a moderately low protein diet, which was otherwise balanced and sufficient in all other nutrients. The secondary hyperparathyroidism persisted after 2 wk of a low protein diet and, in preliminary studies, after 4 wk of the same diet (J. Kerstetter, unpublished observation). We found that a low protein diet induced secondary hyperparathyroidism in men and postmenopausal women as well (62 ). Secondary hyperparathyroidism is defined as the appropriate rise in circulating concentrations of PTH in response to a hypocalcemic challenge.
|
What induces the elevation in serum PTH when protein intake is limited? Because dietary calcium was kept constant and moderate (20–24 mmol) in both our study (22 ) and that of Giannini et al. (63 ), dietary calcium insufficiency is not the explanation. This leaves open the possibilities that intestinal and/or skeletal handling of calcium are altered by a low protein diet.
Most calcium balance studies in humans (7 –12 ,15 ,18 ,60 ) could find no effect of dietary protein on intestinal calcium absorption, although there were three reports to the contrary (6 ,16 ,61 ). Calcium balance studies may not be sufficiently sensitive to detect an effect. Further, given the earliest research of Sherman and McCance (64 ,65 ), in which dietary protein impacted calcium absorption, we decided to revisit the question and employ dual stable calcium isotopes to directly measure intestinal calcium absorption at different levels of dietary protein.
The second study utilized the same experimental protocol described in our first study except that we measured intestinal calcium absorption at d 4 using dual stable calcium isotopes. Seven women completed the study while consuming high (2.1 g protein/kg) and low protein (0.7 g protein/kg) diets and the results were published (25 ). Since then, using precisely the same protocol, we have studied 13 additional healthy women (10 young and 3 postmenopausal). The results of the combined studies of the 20 women are summarized in Figure 3 .
|
8%) explains 80% of the change in urinary calcium excretion between the low and high protein diets (3.4 ± 0.3 to 5.4 ± 0.4 mmol/d, P = 0.000001). Dietary calcium was constant at 20 mmol. Two recent isotopic studies were published that concluded that dietary protein did not affect intestinal calcium absorption (69 ,70 ). The reason for the discrepant results probably lies in the study design. In the Heaney and Dawson-Hughes report (69 ,70 ), calcium absorption was measured while subjects consumed their usual diets, and despite respectable sample sizes, there was no association between calcium absorption and protein intake. The large and natural interindividual variability in calcium absorption (evident from Fig. 3 where subject’s diets were tightly controlled) in combination with other uncontrolled dietary factors likely precluded finding an association between protein and calcium absorption.
In our first study, a protein intake of 0.7 g/kg led to impaired intestinal calcium absorption and secondary hyperparathyroidism, whereas subjects consuming 1.0 g/kg demonstrated little change in calcium homeostasis. Because the range of dietary protein between 0.7 and 1.0 g/kg encompasses the current RDA for this nutrient (0.8 g/kg) (4 ), we next undertook a dose-response study to examine the effect of graded levels of dietary protein (0.7, 0.8, 0.9 and 1.0 g protein/kg) on calcium homeostasis (27 ). Following our standard 4-d experimental model, all four diets were administered randomly to eight healthy young women and the principal findings are summarized in Figure 4 .
|
These dose-dependent data are important for two reasons (27 ). First, they demonstrate that the response to a progressive reduction in dietary protein intake is not a graded phenomenon, but rather a threshold effect, with the abrupt appearance of disordered mineral homeostasis observed at levels of protein intake below 0.9 g/kg. Second, they suggest that in healthy young women consuming a well-balanced, calcium-sufficient diet (20 mmol), the current RDA for protein (0.8 g/kg) results, in at least the short-term, in altered calcium homeostasis.
It is important to recall that the current dietary reference intake (DRI) for calcium for adult women is 25 mmol (71 ), a level higher than the 20 mmol used in our experiments. However, the average calcium intake for U.S. adult women is in the 15–18 mmol range (3 ), slightly less than the 20 mmol used in the experiments. It would be important to know whether the current higher DRI for calcium would ameliorate the secondary hyperparathyroidism induced by the low protein diet. Likewise, we do not know whether the secondary hyperparathyroidism is exacerbated when calcium intake is lower than 20 mmol, which would be the case for almost 80% of adult women in the United States (3 ).
|
The chronic impact of low protein diets |
|---|
|
TOPABSTRACTDietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
Epidemiological studies, taken as a whole, do not satisfactorily answer the question of how chronically low protein diets impact the skeleton. When BMD is the primary outcome, most (39 –48 ), but not all (49 –53 ), epidemiological studies show a positive relationship between protein intake and BMD. Stated another way, most of the epidemiological evidence shows that when other known dietary factors are controlled, those individuals who consume low protein diets have lower BMD. Using the National Health and Nutrition Examination Survey (NHANES) III database, we found that in 1882 non-Hispanic white women 50 y old and older, after adjusting for age and body weight, a low protein intake was associated with a significantly lower hip bone mineral density (Fig. 5 ) (47 ). Consistent with these data, Hannan and colleagues (46 ) studied 615 participants in the Framingham Osteoporosis Study over a 4-y period and found that lower levels of protein intake were associated with significantly higher rates of bone loss at the hip and spine. These findings confirm the earlier work of Freudenheim et al. (39 ), who reported that a low protein intake was associated with greater loss in bone density from the wrist in 35- to 65-y-old women. Most recently, Promislow et al. (48 ) found a positive association between total dietary protein intake and BMD in elderly men and women participating in the Rancho Bernardino study. Therefore, there is substantial agreement in those studies in which BMD is the primary outcome. Munger et al. (59 ), reporting data from the Iowa Women’s Health Study, found an increased risk of hip fracture in 55- to 69-y-old women consuming the lowest amounts of protein. Our observation that low protein intakes reduce intestinal calcium absorption provides a potential pathophysiologic explanation for these epidemiological findings.
|
Adequate dietary protein may also help in fracture healing and in preventing bone loss after fracture. Bonjour and colleagues (73
) studied the effects of 6 mo of protein supplementation, after osteoporotic hip fracture, in a group of elderly subjects. These patients had self-selected protein intakes that were very low (40 g). The administration of additional protein (+20 g) was associated with significant attenuation of proximal femur bone loss in the fractured hip such that, at 1 y, bone loss rates were 50% lower in the protein-supplemented individuals. The correction of poor protein nutrition also improved serum prealbumin and insulin-like growth factor 1 (IGF-1) concentrations and decreased the length of rehabilitation (73
).
|
Summary and conclusions |
|---|
|
TOPABSTRACTDietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
Bone is complex tissue that changes slowly. As such, it is difficult to design and conduct well-controlled nutrition studies in humans to quantify the effect of one nutrient on bone. However, given the increasing prevalence of osteoporosis and the clear impact of dietary protein on calcium metabolism, it is imperative that we gain a better understanding of the complex interplay between dietary protein and skeletal health. Toward that end, longer-term physiologic studies and, eventually, dietary intervention studies will be required to provide better-informed dietary protein guidelines for optimal skeletal health.
|
FOOTNOTES |
|---|
2 This work was supported by grants from the U.S. Department of Agriculture (00-35200-9579, 97-35200-4420, 94-37200-0668), the National Institutes of Health (DK52128-03, NIH MO1-RR00125, NIH 5P30AR46032-04), the Catherine Weldon Donaghue Women’s Health Investigator Program at Yale University and the University of Connecticut.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTDietary protein and calcium...The traditional viewThe acute impact of...The chronic impact of...Summary and conclusionsLITERATURE CITED |
|---|
1. National Osteoporosis Foundation (2002) Osteoporosis, Disease Statistics. 2002(Website accessed September 2002, www.nof.org).
2. Barzel, U. S. & Massey, L. K. (1998) Excess dietary protein can adversely affect bone. J. Nutr. 128:1051-1053.
3. Food Surveys Research Group, Beltsville Human Nutrition Research Center, Agricultural Research Service (1999) Supplementary Data Tables, USDA’s 1994–1996 Continuing Survey of Food Intakes by Individuals 1999 U.S. Department of Agriculture Riverdale, MD.
4. Standing Committee on the Scientific Evaluation of Dietary Reference Intakes Food and Nutrition Board Institute of Medicine (2002) Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Protein and Amino Acids (Macronutrients) 2002 National Academy Press Washington, DC.
5. Johnson, N. E., Alcantara, E. N. & Linkswiler, H. (1970) Effect of level of protein intake on urinary and fecal calcium and calcium retention of young adult males. J. Nutr. 100:1425-1430.
6. Walker, R. M. & Linkswiler, H. M. (1972) Calcium retention in the adult human male as affected by protein intake. J. Nutr. 102:1297-1302.
7. Anand, C. R. & Linkswiler, H. M. (1974) Effect of protein intake on calcium balance of young men given 500 mg calcium daily. J. Nutr. 104:695-700.
8. Allen, L. H., Oddoye, E. A. & Margen, S. (1979) Protein-induced hypercalciuria: a longer term study. Am. J. Clin. Nutr. 32:741-749.
9. Schuette, S. A., Zemel, M. B. & Linkswiler, H. M. (1980) Studies on the mechanism of protein-induced hypercalciuria in older men and women. J. Nutr. 110:305-315.
10. Hegsted, M. & Linkswiler, H. M. (1981) Long-term effects of level of protein intake on calcium metabolism in young adult women. J. Nutr. 111:244-251.
11. Hegsted, M., Schuette, S. A., Zemel, M. B. & Linkswiler, H. M. (1981) Urinary calcium and calcium balance in young men as affected by level of protein and phosphorus intake. J. Nutr. 111:553-562.
12. Spencer, H., Kramer, L., DeBartolo, M., Norris, C. & Osis, D. (1983) Further studies of the effect of a high protein diet as meat on calcium metabolism. Am. J. Clin. Nutr. 37:924-929.
13. Spencer, H., Kramer, L., Osis, D. & Norris, C. (1978) Effect of a high protein (meat) intake on calcium metabolism in man. Am. J. Clin. Nutr. 31:2167-2180.
14. Chu, J. Y., Margen, S. & Costa, F. M. (1975) Studies in calcium metabolism. II. Effects of low calcium and variable protein intake on human calcium metabolism. Am. J. Clin. Nutr. 28:1028-1035.
15. Kim, Y. & Linkswiler, H. M. (1979) Effect of level of protein intake on calcium metabolism and on parathyroid and renal function in the adult human male. J. Nutr. 109:1399-1404.
16. Lutz, J. & Linkswiler, H. M. (1981) Calcium metabolism in postmenopausal and osteoporotic women consuming two levels of dietary protein. Am. J. Clin. Nutr. 34:2178-2186.
17. Schuette, S. A., Hegsted, M., Zemel, M. B. & Linkswiler, H. M. (1981) Renal acid, urinary cyclic AMP, and hydroxyproline excretion as affected by level of protein, sulfur amino acid and phosphorus intake. J. Nutr. 111:2106-2116.
18. Schuette, S. A. & Linkswiler, H. M. (1982) Effects on Ca and P metabolism in humans by adding meat, meat plus mild, or purified proteins plus Ca and P to a low protein diet. J. Nutr. 112:338-349.
19. Draper, H. H., Piche, L. A. & Gibson, R. S. (1991) Effects of a high protein intake from common foods on calcium metabolism in a cohort of postmenopausal women. Nutr. Res. 11:273-281.
20. Lutz, J. (1984) Calcium balance and acid-base status of women as affected by increased protein intake and by sodium bicarbonate ingestion. Am. J. Clin. Nutr. 39:281-288.
21. Trilok, G. & Draper, H. H. (1989) Sources of protein-induced endogenous acid production and excretion by human adults. Calcif. Tissue. Int. 44:335-338.[Medline]
22. Kerstetter, J. E., Caseria, D. D., Mitnick, M. E., Ellison, A. F., Gay, L. F., Liskov, T. A., Carpenter, T. O. & Insogna, K. L. (1997) Increased circulating concentrations of parathyroid hormone in healthy, young women consuming a protein-restricted diet. Am. J. Clin. Nutr. 66:1188-1196.
23. Shapses, S. A., Robins, S. P., Schwartz, E. I. & Chowdhury, H. (1995) Short-term changes in calcium but not protein intake alter the rate of bone resorption in healthy subjects as assessed by urinary pyridinium cross-link excretion. J. Nutr. 125:2814-2821.
24. Mahalko, J. R., Sandstead, H. H., Johnson, L. K. & Milne, D. B. (1983) Effect of a moderate increase in dietary protein on the retention and excretion of Ca, Cu, Fe, Mg, P, and Zn by adult males. Am. J. Clin. Nutr. 37:8-14.
25. Kerstetter, J. E., O’Brien, K. O. & Insogna, K. L. (1998) Dietary protein affects intestinal calcium absorption. Am. J. Clin. Nutr. 68:859-865.[Abstract]
26. Zemel, M. B., Schuette, S. A., Hegsted, M. & Linkswiler, H. M. (1981) Role of the sulfur-containing amino acids in protein-induced hypercalciuria in men. J. Nutr. 111:545-552.
27. Kerstetter, J., Svastisalee, C., Caseria, D., Mitnick, M. & Insogna, K. (2000) A threshold for low-protein-diet-induced elevations in parathyroid hormone. Am. J. Clin. Nutr. 72:168-173.
28. Licata, A. A. (1981) Acute effects of increased meat protein on urinary electrolytes and cyclic adenosine monophosphate and serum parathyroid hormone. Am. J. Clin. Nutr. 34:1779-1784.
29. Margen, S., Chu, J. Y., Kaufmann, N. A. & Calloway, D. H. (1974) Studies in calcium metabolism. I. The calciuretic effect of dietary protein. Am. J. Clin. Nutr. 27:584-589.[Abstract]
30. Pannemans, D. L., Schaafsma, G. & Westerterp, K. R. (1997) Calcium excretion, apparent calcium absorption and calcium balance in young and elderly subjects: influence of protein intake. Br. J. Nutr. 77:721-729.[Medline]
31. Zemel, M. B. (1988) Calcium utilization: effect of varying level and source of dietary protein. Am. J. Clin. Nutr. 48:880-883.
32. Remer, T. (2000) Influence of diet on acid–base balance. Semin. Dial. 13:221-226.[Medline]
33. Remer, T. & Manz, F. (1995) Potential renal acid load of foods and its influence on urine pH. J. Am. Diet. Assoc. 95:791-797.[Medline]
34. Bushinsky, D. A. (1996) Metabolic alkalosis decreases bone calcium efflux by suppressing osteoclasts and stimulating osteoblasts. Am. J. Physiol. Renal Fluid Electrolyte Physiol. 271:F216-F222.
35. Arnett, T. R. & Spowage, M. (1996) Modulation of the resorptive activity of rat osteoclasts by small changes in extracellular pH near the physiological range. Bone 18:277-279.[Medline]
36. Bushinsky, D. A., Parker, W. R., Alexander, K. M. & Krieger, N. S. (2001) Metabolic, but not respiratory, acidosis increases bone PGE(2) levels and calcium release. Am. J. Physiol. Renal Fluid Electrolyte Physiol. 281:F1058-F1066.
37. Barzel, U. S. & Jowsey, J. (1969) The effects of chronic acid and alkali administration on bone turnover in adult rats. Clin. Sci. 36:517-524.[Medline]
38. Sebastian, A., Harris, S. T., Ottaway, J. H., Todd, K. M. & Morris, R. C., Jr (1994) Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate. N. Engl. J. Med. 330:1776-1781.
39. Freudenheim, J. L., Johnson, N. E. & Smith, E. L. (1986) Relationships between usual nutrient intake and bone-mineral content of women 35–65 years of age: longitudinal and cross-sectional analysis. Am. J. Clin. Nutr. 44:863-876.
40. Teegarden, D., Lyle, R. M., McCabe, G. P., McCabe, L. D., Proulx, W. R., Michon, K., Knight, A. P., Johnston, C. C. & Weaver, C. M. (1998) Dietary calcium, protein, and phosphorus are related to bone mineral density and content in young women. Am. J. Clin. Nutr. 68:749-754.[Abstract]
41. Lacey, J. M., Anderson, J. J., Fujita, T., Yoshimoto, Y., Fukase, M., Tsuchie, S. & Koch, G. G. (1991) Correlates of cortical bone mass among premenopausal and postmenopausal Japanese women. J. Bone Miner. Res. 6:651-659.[Medline]
42. Geinoz, G., Rapin, C. H., Rizzoli, R., Kraemer, R., Buchs, B., Slosman, D., Michel, J. P. & Bonjour, J. P. (1993) Relationship between bone mineral density and dietary intakes in the elderly. Osteoporos. Int. 3:242-248.[Medline]
43. Cooper, C., Atkinson, E. J., Hensrud, D. D., Wahner, H. W., O’Fallon, W. M., Riggs, B. L. & Melton, L. J., 3rd (1996) Dietary protein intake and bone mass in women. Calcif. Tissue Int. 58:320-325.[Medline]
44. Chiu, J. F., Lan, S. J., Yang, C. Y., Wang, P. W., Yao, W. J., Su, L. H. & Hsieh, C. C. (1997) Long-term vegetarian diet and bone mineral density in postmenopausal Taiwanese women. Calcif. Tissue Int. 60:245-249.[Medline]
45. Lau, E. M., Kwok, T., Woo, J. & Ho, S. C. (1998) Bone mineral density in Chinese elderly female vegetarians, vegans, lacto-vegetarians and omnivores. Eur. J. Clin. Nutr. 52:60-64.[Medline]
46. Hannan, M. T., Tucker, K. L., Dawson-Hughes, B., Cupples, L. A., Felson, D. T. & Kiel, D. P. (2000) Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. J. Bone Miner. Res. 15:2504-2512.[Medline]
47. Kerstetter, J. E., Looker, A. C. & Insogna, K. L. (2000) Low protein intake and low bone density. Calcif. Tissue. Int. 66:313.[Medline]
48. Promislow, J. H., Goodman-Gruen, D., Slymen, D. J. & Barrett-Connor, E. (2002) Protein consumption and bone mineral density in the elderly: the Rancho Bernardo Study. Am. J. Epidemiol. 155:636-644.
49. Metz, J. A., Anderson, J. J. & Gallagher, P. N., Jr (1993) Intakes of calcium, phosphorus, and protein, and physical-activity level are related to radial bone mass in young adult women. Am. J. Clin. Nutr. 58:537-542.
50. Mazess, R. B. & Barden, H. S. (1991) Bone density in premenopausal women: effects of age, dietary intake, physical activity, smoking, and birth-control pills. Am. J. Clin. Nutr. 53:132-142.
51. Nieves, J. W., Golden, A. L., Siris, E., Kelsey, J. L. & Lindsay, R. (1995) Teenage and current calcium intake are related to bone mineral density of the hip and forearm in women aged 30–39 years. Am. J. Epidemiol. 141:342-351.
52. Henderson, N. K., Price, R. I., Cole, J. H., Gutteridge, D. H. & Bhagat, C. I. (1995) Bone density in young women is associated with body weight and muscle strength but not dietary intakes. J. Bone Miner. Res. 10:384-393.[Medline]
53. Wang, M. C., Luz Villa, M., Marcus, R. & Kelsey, J. L. (1997) Associations of vitamin C, calcium and protein with bone mass in postmenopausal Mexican American women. Osteoporos. Int. 7:533-538.[Medline]
54. Kerstetter, J. E., Mitnick, M. E., Gundberg, C. M., Caseria, D. M., Ellison, A. F., Carpenter, T. O. & Insogna, K. L. (1999) Changes in bone turnover in young women consuming different levels of dietary protein. J. Clin. Endocrinol. Metab. 84:1052-1055.
55. Abelow, B., Holford, T. & Insogna, K. (1992) Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calcif. Tissue Int. 50:14-18.[Medline]
56. Feskanich, D., Willett, W. C., Stampfer, M. J. & Colditz, G. A. (1996) Protein consumption and bone fractures in women. Am. J. Epidemiol. 143:472-479.
57. Meyer, H. E., Pedersen, J. I., Loken, E. B. & Tverdal, A. (1997) Dietary factors and the incidence of hip fracture in middle-aged Norwegians. A prospective study. Am. J. Epidemiol. 145:117-123.
58. Frassetto, L. A., Todd, K. M., Morris, R. C., Jr & Sebastian, A. (2000) Worldwide incidence of hip fracture in elderly women: relation to consumption of animal and vegetable foods. J. Gerontol. A Biol. Sci. Med. Sci. 55:M585-M592.
59. Munger, R. G., Cerhan, J. R. & Chiu, B. C. (1999) Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am. J. Clin. Nutr. 69:147-152.
60. Heaney, R. P. & Recker, R. R. (1982) Effects of nitrogen, phosphorus, and caffeine on calcium balance in women. J. Lab. Clin. Med. 99:46-55.[Medline]
61. Kaneko, K., Masaki, U., Aikyo, M., Yabuki, K., Haga, A., Matoba, C., Sasaki, H. & Koike, G. (1990) Urinary calcium and calcium balance in young women affected by high protein diet of soy protein isolate and adding sulfur-containing amino acids and/or potassium. J. Nutr. Sci. Vitaminol. (Tokyo) 36:105-116.
62. Kerstetter, J. E., Svastisalee, C. M., Mitnick, M. E., Caseria, D. M. & Insogna, K. L. (2000) Dietary protein-induced changes in mineral metabolism are not influenced by age or sex. J Bone Miner. Res. 15:S423(abs.).
63. Giannini, S., Nobile, M., Sartori, L., Dalle Carbonare, L., Ciuffreda, M., Corro, P., D’Angelo, A., Calo, L. & Crepaldi, G. (1999) Acute effects of moderate dietary protein restriction in patients with idiopathic hypercalciuria and calcium nephrolithiasis. Am. J. Clin. Nutr. 69:267-271.
64. Sherman, H. (1920) Calcium requirement of maintenance in man. J. Biol. Chem. 44:21-27.
65. McCance, R. A., Widdowson, E. M. & Lehmann, H. (1942) The effect of protein intake on the absorption of calcium and magnesium. Biochem. J. 36:686.
66. Heaney, R. P., Weaver, C. M., Fitzsimmons, M. L. & Recker, R. R. (1990) Calcium absorptive consistency. J. Bone Miner. Res. 5:1139-1142.[Medline]
67. Heaney, R. P. & Recker, R. R. (1986) Distribution of calcium absorption in middle-aged women. Am. J. Clin. Nutr. 43:299-305.
68. Heaney, R. P. (1999) Absorbing calcium. Clin. Chem. 45:161-162.
69. Heaney, R. P. (2000) Dietary protein and phosphorus do not affect calcium absorption. Am. J. Clin. Nutr. 72:758-761.
70. Dawson-Hughes, B. & Harris, S. S. (2002) Calcium intake influences the association of protein intake with rates of bone loss in elderly men and women. Am. J. Clin. Nutr. 75:773-779.
71. Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine (1997) Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D and Fluoride 1997 National Academy Press Washington, DC.
72. Hegsted, D. M. (1986) Calcium and osteoporosis. J. Nutr. 116:2316-2319.
73. Schurch, M. A., Rizzoli, R., Slosman, D., Vadas, L., Vergnaud, P. & Bonjour, J. P. (1998) 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. 128:801-809.
This article has been cited by other articles:
|
|
 |
|
  M. P. Thorpe, E. H. Jacobson, D. K. Layman, X. He, P. M. Kris-Etherton, and E. M. Evans 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., June 1, 2008; 138(6): 1096 - 1100. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Thorpe, M. C. Mojtahedi, K. Chapman-Novakofski, E. McAuley, and E. M. Evans A Positive Association of Lumbar Spine Bone Mineral Density with Dietary Protein Is Suppressed by a Negative Association with Protein Sulfur J. Nutr., January 1, 2008; 138(1): 80 - 85. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. F. W. Kin, W. S. Y. Shan, L. J. C. Shun, L. P. Chung, and W. Jean Experience of famine and bone health in post-menopausal women Int. J. Epidemiol., October 1, 2007; 36(5): 1143 - 1150. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Contaldo and F. Pasanisi High-protein diet, obesity, and the environment Am. J. Clinical Nutrition, February 1, 2006; 83(2): 387 - 387. [Full Text] [PDF]
|
|
|
|
|
|
K. Nakamura, K. Ueno, T. Nishiwaki, Y. Okuda, T. Saito, Y. Tsuchiya, and M. Yamamoto Nutrition, mild hyperparathyroidism, and bone mineral density in young Japanese women Am. J. Clinical Nutrition, November 1, 2005; 82(5): 1127 - 1133. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Devine, I. M Dick, A. F. Islam, S. S Dhaliwal, and R. L Prince Protein consumption is an important predictor of lower limb bone mass in elderly women Am. J. Clinical Nutrition, June 1, 2005; 81(6): 1423 - 1428. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. W. Campbell, J. C. Fleet, R. T. Hall, and N. S. Carnell Short-Term Low-Protein Intake Does Not Increase Serum Parathyroid Hormone Concentration in Humans J. Nutr., August 1, 2004; 134(8): 1900 - 1904. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E Kerstetter, K. O O'Brien, and K. L Insogna Dietary protein, calcium metabolism, and skeletal homeostasis revisited Am. J. Clinical Nutrition, September 1, 2003; 78(3): 584S - 592. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. K. Massey Dietary Animal and Plant Protein and Human Bone Health: A Whole Foods Approach J. Nutr., March 1, 2003; 133(3): 862S - 865. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
