Asia Pacific J Clin Nutr (1993) 2, 183-190

Requirements of calcium: are there ethnic differences?

Warren Tak-keung Lee BSc (Hum Nutr) (Dublin), MPhil (CUHK), PhD Candidate (CUHK), SRD (UK)

Research Dietitian, Growth and Nutrition Research Team, Department of Paediatrics, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, Hong Kong.

Calcium is an essential dietary element to maintain the integrity of the skeleton. A higher peak adult bone mass has been shown to reduce the risk of osteoporotic fractures later in life. It is postulated that a lifelong higher calcium intake would reduce bone loss in advancing age. Available scientific evidence seems to indicate that within any ethnic group, calcium intake is positively associated with bone mass. Controlled calcium supplementation trials in both low and high dietary calcium intake children and adolescents showed that there is an association between calcium intake and gains in bone mass. Furthermore, studies in adolescents showed that genetic inheritance and skeletal responses to hormonal changes at puberty have great influences on bone mass increments in addition to calcium intake. Interestingly, across-cultural comparisons are not convincing enough to demonstrate that lower calcium intake would predispose to higher risk of osteoporosis. It implies that the genetic inheritance and complex environmental factors may be important modulators on bone mass achievement in addition to calcium intake within any ethnic group. There are pitfalls in the current Recommended Dietary Allowances (RDAs) for calcium which are usually based on clinical studies conducted in Caucasians with higher calcium intakes and the extent of nutritional adaptation to low calcium intake is ignored. Given the fact that there are ethnic differences in calcium absorption, dietary habits, bone metabolism, physical activity and skeletal size as well as body build, the requirements of calcium in Asians may be different from Caucasians. Ideally, each nation should establish its own RDA based on the ethnic make-up of its population. In Asian countries, the major sources of calcium are derived from vegetable types of foods, fish and shell fish with edible bones, fins and shells, etc. Recent absorption studies in humans with low-oxalate and low-phytate vegetables and pulses also showed that contrary to common presuppositions, these vegetables with low calcium chelators do have a comparable calcium absorbability to milk. Studies on bioavailability of calcium from Asian foods and diets are warranted in order to identify rich sources of calcium.

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Introduction

The rising incidence of osteoporotic fractures is becoming a global public health problem. Currently, medical therapies for osteoporosis only help to retard the rate of bone loss but cannot help to regain the bone that is lost. The achievement of a higher bone mass by increasing calcium intake throughout life is considered to be a better preventive measure to prevent the risk of developing osteoporosis later in life^1,2. However, there is no unequivocal evidence across cultures to support the contention that a lifelong higher calcium intake is associated with a lower risk of developing osteoporotic fractures.

Calcium and bone mass

Over 99% of body calcium is stored in the skeleton in the form of calcium phosphate. Body calcium salts form an architectural framework to maintain skeletal integrity, less than 1% of calcium is in an ionized form or bound to proteins in the extracellular fluid, in which calcium is actively involved in vital biochemical processes namely, cell membrane permeability, nerve conduction, cardiac and muscle contraction and blood coagulation³. If there is a chronic insufficiency of calcium intake, calcium will be resorbed from the skeleton, a calcium reservoir, into the extracellular fluid to maintain its concentration such that the vital processes can be maintained^4,5

Bone is a dynamic tissue inside which there is a continuous process of bone turnover characterized by ongoing bone formation coupled with resorption. During the years of growth bone formation exceeds resorption, body calcium accretion increases from 30g at birth to 850-1400g in adulthood as a result of net bone formation⁶. The rates of skeletal calcium accretion vary at different stages of life. During the first six months of life, the daily calcium accretion in the skeleton is rapid at 150-200mg/d, with less influx in mid-childhood years (75-100mg/d), and up to 400mg/d during puberty growth spurt in adolescence⁷.

The process of bone formation does not terminate after cessation of linear growth, consolidation of bone mass continues until 'peak bone mass' is achieved in the second decade to the third decade of life²; however, the timing is varied in different ethnic groups^8-10, Genetic inheritance accounts for 70-80% of the attainment in peak bone mass^11-13, whereas body build^14-17 including lean body mass^18-19; physical activity^18,20-22; dietary intake including calcium^22-25, protein^26-28, phosphorus^26,29 and sodium^30,31; smoking^32,33 and alcohol consumption^22,34, etc are modifiable environmental factors that may determine the remaining 20-30% variation in peak bone mass. The amount of peak bone mass varies in different ethnic groups at skeletal maturity too. Black Africans have a relatively higher amount of bone mass compared with Caucasians^35-37, whereas there is some evidence that Orientals^38,25 have a relatively lower bone mass when compared with Caucasians³⁹, despite the fact that Oriental people were often reported to have lifetime lower bone mass and body frame than Caucasians^40-42.

In contrast, the incidence of fractures in Oriental women were reported much lower than Caucasian women⁴⁰ who have relatively higher bone mass. A recent cross-sectional study²⁵ in over 840 women at aged 35-75 years from 5 rural counties of Mainland China where mean calcium intakes varied from 230-720mg/d showed that nearly all the study women over the age of 50 had bone mass less than the fracture threshold point which is specifically for the U.S. Caucasian women⁴³. However, a majority of these Chinese subjects had not experienced any signs of osteoporosis or episodes of osteoporotic fractures in their life. Less than 4% of the study women reported incidents of fractures in their life. This fracture rate is much lower than those reported in Caucasian populations^44,45. The low fracture incidence in this investigation was consistent with those reports in Chinese populations of Hong Kong and Singapore⁴⁰. It is postulated that other risk factors besides bone mass and body frame, such as hereditary factors, dietary constituents, physical activity and the risk of fall may be important to explain the difference in prevalence of fracture. Oriental people usually have smaller body frame and skeletal mass than Caucasians, it is logical to consider that less mechanical stress, hence lower bone mass, may be required by Oriental women to support their smaller body weight when compared with Caucasians. In fact, studies have shown that racial difference in bone density disappeared after confounding factors of body weight and height were controlled in comparing ethnic differences in bone density^9,46.

It is a universal phenomenon that bone mass after reaching the peak gradually declines when the process of bone degradation predominates in older age. Although the loss of bone mass occurs both in men and women with advancing age, the rate of decline in women is greater due to accelerated bone loss after menopause as a result of deficient in production of estrogen which is a major protective factor to maintain positive bone turnover in women⁴⁷. The phenomenon of age-related bone loss is believed to be associated with several factors an increased bone resorption mediated by estrogen deficiency⁴⁷, age-related decline in intestinal calcium absorption^48,49, and a fall in the hydroxylation of 1,25dihydroxyvitamin D₃ in the elderly due to age-related fall in renal function⁵⁰. However, other workers reported normal 1,25-dihydroxyvitamin D₃ level in the elderly^51,52 including elderly Chinese women⁵³. Osteoporotic fractures may occur in individuals when bone mass falls below a certain threshold level^43,48,54. Adults with average bone mass less than the population mean in which he/she belongs to during skeletal maturity may be at a higher risk of osteoporosis later in life^54,55. Hu and co-workers, however, showed that the fracture threshold level for Chinese women²⁵ may be lower than women in western countries^43,54. Osteoporosis in men in general occurs more frequently over 70⁴⁸.

Calcium intakes and requirements

Many nations recommend specific amounts of calcium as reference intakes for the normal healthy populations. Recommended Dietary Allowance (RDA) of calcium is the quantity of calcium to be consumed on a regular basis for the maintenance of health and the prevention of calcium deficiency diseases, the RDA should also take into account the known environmental dietary and morbidity characteristics of the nation concerned. Thus, caution should be taken to apply RDA from one particular ethnic group to another. Furthermore, the scientific basis which national RDA figures are based, should be carefully scrutinized. For example, the US RDA for calcium has been traditionally set at two standard deviations above the mean requirements which aims at providing a wide margin of safety above the needs for the majority of the population in the US⁵⁶. It is believed that an ample food supply in the US should be able to meet the escalated requirements without difficulty⁵⁷. Consequently, the levels of RDA for calcium in the US may be inflated and may not necessarily indicate the actual mean requirements of the population. In the US, there is also a suggestion to further increase the current calcium RDA (800mg/d) by about 50% during adulthood as a prophylactic means to reduce the risk of developing osteoporosis¹.

Calcium intakes of the world populations vary a great deal. In countries with dairy farming, average calcium intake may be as high as 1000mg/d or even higher, whereas in communities where animal milks are not available or not traditionally consumed, habitual calcium intakes are often below the recommended amounts of 500mg/d^58,59. Ironically, epidemiological data have shown that the incidence of osteoporosis is lower in some regions of the world where milk is not customarily consumed and therefore calcium intake is low^9,60,61. No convincing data have shown that populations subsisting on habitual lower calcium diets would hamper the general health and bone growth^62-65, except individual cases of rickets occurring in African children associated with lifelong extremely low calcium intakes^66,67.

Calcium requirements in adulthood

The RDA for calcium varies from 400mg/d⁵⁸ to 800mg/ d⁶⁸. Calcium requirements in adults are determined by the amount of calcium needed to promote consolidation of the skeleton after cessation of linear growth, and to compensate for obligatory losses in the intestine, kidney and skin.

Early studies in adults accustomed to low calcium diets shows that humans are capable of adapting to a low calcium intake by enhancing intestinal calcium absorption and reducing urinary calcium excretion^69-71. The success of adaptation is mediated by increased serum level of parathyroid hormone and vitamin D to facilitate the uptake of calcium in the intestine^69,72,73 and to reduce obligatory urinary calcium excretion^23,69,74. When subjects accustomed to daily calcium diet of about 1000mg, a sudden reduction of calcium intake by half would lead to negative balance, although full adaptation occurred with positive calcium retention several months later⁷⁰. In fact, very few current calcium RDAs are based on balanced studies in populations with lifelong low calcium intakes⁵⁸.

In western societies, the estimates of calcium requirements are based on balance studies of higher calcium intake individuals⁵⁹. These estimations do not address the ability of the body to adapt various levels of calcium intakes. In fact, the amount of calcium required to maintain positive balance depends on previous calcium intakes, and a high habitual calcium intake requires higher requirement of calcium to maintain positive balance^75,76. Due to this adaptive response, calcium requirements cannot be simply determined by estimating positive calcium balance at various levels of intakes over a relatively short period of time unless the period of the balance study is sufficiently prolonged such that full adaptation can be assured. Therefore, estimation of calcium requirements based on a sudden decrease in calcium intake as found in most traditional balance studies is liable to errors⁶³. Today, with an advancement in the technique of non-radioactive stable isotopes⁷⁷, calcium requirements can be determined in individuals from infancy to elderly with self-selected diets without the shortcomings incurred in traditional balance studies^77,78.

Furthermore, calcium requirements can be modified by dietary factors: a habitually higher calcium diet renders a lower calcium absorption and vice versa⁷¹. Certain amino acids and complex sugars are known to facilitate calcium absorption, whereas chelators such as oxalic acid and phytic acid, dietary fibres, and unabsorbed organic phosphates may inhibit calcium bioavailability in the gut⁷⁹. In addition, high intakes of protein and sodium are proven to induce a higher urinary calcium loss^80,81. In affluent societies a greater allowance for calcium intakes is recommended because of the high consumption of animal protein and sodium. In summary, determinants of calcium retention are multifactorial, with a complex interaction between genetic, dietary and other lifestyle factors. As a result, caution should be exercised when adopting recommendations which are based on specific ethnic populations with specific food cultures and lifestyles.

Calcium requirements in childhood

The calcium RDAs for children around the world vary from 400mg/d to 1000mg/d⁵⁹ reflecting that there is no agreed consensus among the expert groups on the optimum calcium requirements for children. In children and adolescents, calcium requirements are mainly determined by two major factors, namely the rate of calcium absorption and the daily skeletal calcium accretion^68,82. The U.S. RDA assumes that calcium absorption in Caucasian children is less than 40%⁶⁸. Furthermore, two recent absorption studies in Caucasian adolescents demonstrated that calcium absorption of adolescents is no different from their adults (less than 40%)^83,84. In contrast, our recent study in Chinese children, those with a usual calcium intake of 300mg/d showed a rate of true absorption to be 63%, whereas that of children with habitual calcium intake at 860mg/d was less at 55%⁸⁵. The results agree with earlier balance studies in low calcium intake Indian and Sri Lankin children that children could adapt to calcium intake at around 300mg/d and were able to maintain positive calcium retention^74,86. The net calcium absorption of rural Indian children subsisting on a diet as low as 200mg/d could reach about 50%, and the urinary calcium loss was at minimal^74,86. These absorption studies suggest that there may be an ethnic difference in calcium absorption. The capability of enhancing calcium absorptive efficiency in some ethnic populations may be inherited from their ancestors who might have adapted successfully to low calcium diets for many generations.

An estimation of daily calcium increments in the skeleton is another key factor in evaluating calcium requirements in growing children. There is evidence to support that there are ethnic differences in bone mineral accretion in children and adolescents³⁶. Several expert groups^68,82,87 devised calcium RDA for children based on the predictive values of daily skeletal calcium increments using the anthropometric data of British children and adolescents in the early 1990s⁷. One of the major pitfalls in this study⁷ is an assumption that calcium increments in the skeleton at different ages are proportional to the increase in body weight during growth, these data may no longer be valid. In addition, these calculated values also relied on an estimation of skeletal calcium content derived from a limited number of young individuals at post-mortem. Given the fact that the skeletal size of Chinese is in general smaller than Caucasians³⁸, it follows that the annual deposition of calcium in the skeleton during growth in the Chinese children and adolescents would also be lower in comparison. As a result, the daily bone mineral accretion rate in Chinese children may be less than the Caucasian children and adolescents. Therefore, the values derived from Caucasians may not be applicable to Chinese populations. As a result, enhanced rates of calcium absorption together with seemingly less daily bone mineral accretion in the Chinese children, the requirements of calcium for Chinese children may be lower than those recommended for American children⁶⁸.

Other factors affecting bone mass differences between ethnic groups

Several population studies have shown that there is a correlation between habitual calcium intake and bone mass within the same ethnic group^88-94. Two recent randomized double blind controlled calcium supplementation trials in pre-pubertal children conducted in China⁶⁵ and the USA⁹⁵ together showed that prepubertal children with either high or low baseline calcium intakes had additional gains in bone mass after receiving supplemental calcium. However, Johnston and coworkers⁹⁵ could not find any significant effect of calcium supplementation on the difference in gain of bone density among 23 pairs of pubertal or post-pubertal twin children. The authors commented that a larger sample size was required to test the effect of supplementation, or the results might imply that hormonal changes during sexual maturity in adolescents override the benefits of calcium supplementation on bone mass increase. Nevertheless, a more recent 18-month calcium supplementation study in 94 Caucasian adolescent girls confirms the effect of calcium supplementation on total bone acquisition in healthy adolescent girls²⁴.

It is interesting to note that cross culturally, bone mass differs between different ethnic groups even if calcium intake and lifestyles are similar^96,97. The acquisition of bone mineral accelerates dramatically due to increased production of sex hormones during the progression of puberty until sexual maturity is reached^10,14,98-100. Gilsanz³⁶ studied the influence of hormonal and hereditary factors on bone mineral accretions in black and white adolescent girls. The spinal bone mass of prepubertal black girls and white girls were not different significantly; however, at the onset of puberty, black girls increased bone mass by 34%, whereas white girls only increased by 11%. This observation provides strong evidence of inheritability in modulating bone mass acquisition. The authors speculated that differences in the production of estrogen and other hormones as well as the differences in sensitivity of the bone to these hormones between black and white adolescents may explain for this discrepancy. Ethnic differences in bone mass are not confined to black and white populations. Garn³⁸ found that Chinese and Japanese had significantly less cortical bone mass than Caucasians. Polynesians with similar or even lower calcium diets have higher bone mass than New Zealand Caucasians⁹⁷.

The results of controlled intervention studies in children and adolescents so far seem to indicate that within a particular ethnic group, increasing calcium intake tends to increase bone mass in children^65,95 and adolescents²⁴. Significant correlations between habitual calcium intakes and bone density are also found in adults of the same ethnicity^25,89,90.94. However, a positive association between calcium intake and bone mass is not usually seen in cross-cultural comparisons^60,96. As it has been discussed previously, there are ethnic differences in body size, peak bone mass achievement, sensitivity of bone to hormonal changes at sexual maturity, efficiency of calcium absorption, dietary intake and physical activity; therefore, the derivation of calcium RDA based on one ethnic group, predominantly Caucasians, may not apply to other ethnic populations.

Available evidence gathered so far appears to indicate that the optimum requirements of calcium in order to achieve optimum bone mass may vary from ethnic group to ethnic group depending on the systemic controls on calcium metabolism and the environmental conditions to which the individuals adapt. As a result, the calcium RDAs for Asian populations, who have lower calcium intake due to lower animal milk consumption, may not be as high as those recommended in the western societies. Promotion of milk consumption in a nation in which people do not traditionally or customarily consume milk may have a significant impact on food culture, agricultural practice and health status. More importantly, taking higher doses of calcium supplements above the RDAs to prevent osteoporosis may interfere iron and zinc absorptions^101,102, and may predispose to the risk of developing urolithiasis¹⁰³. More research is needed in the eastern world to determine the optimum calcium requirements.

Bioavailability of calcium from milk and plant foods

It is indisputable that milk and milk products are rich sources of calcium, the absence of calcium chelators such as oxalate and phytate in milk renders its calcium more available for absorption. Popular nutrition textbooks state that calcium from plant foods: dark green leafy vegetables, beans and pulses are poorly available for absorption. Oxalate in vegetables and phytate in beans and pulses may form insoluble compounds with calcium which are unavailable for absorption^104,105. A recent clinical study in humans¹⁰⁶ shows that calcium absorption in low-oxalate and high-calcium dark green leafy vegetables belonging to the family of Brassica is comparable to milk. Kale, broccoli, mustard green, Chinese kale and dark green Chinese cabbage are examples in that family In addition, another recent absorption study in humans also showed that calcium absorption from low-phytate content soy bean and products compares favourably with milk¹⁰⁷. The results of these recent absorption studies in humans confirm that not all plant foods contain calcium chelators. Thus, calcium absorption is preserved in a wide variety of plant foods low in oxalate and phytate. The rates of calcium absorption in some of these foods may be comparable with milk. In fact, beans, pulses, dark green leafy vegetables, are the main source of calcium in the diets of Mainland Chinese. In addition, edible seeds, fish with edible bones and fins, soft-bones of poultry are potential sources of calcium in the Chinese diets, studying their bioavailability would be a worthwhile pursuit.

Conclusion

In conclusion, more local research should be carried out among indigenous Asian populations in the areas of calcium adaptation, peak bone mass attainment and related modulating factors such as calcium absorption and bioavailability of calcium from the traditional diets in order to establish a more reliable and practical RDA. In fact, a concern for ethnic difference in calcium requirement has been reflected in a recent Consensus Development Conference on Osteoporosis held in Hong Kong, April, 1993, which was organized by the American and European Foundations for Osteoporosis and Bone Diseases and the National Institute of Arthritis and Musculoskeletal and Skin Diseases of the USA. The consensus statements consider ethnic difference in calcium requirements is an important factor to formulate future RDAs for the world populations: '.... requirements (calcium) may differ in other ethnic groups and may be less in people with lower protein intakes and small skeletal size....'

*Based on a paper presented at the 'Milk of Life' seminar organized by the Danish Dairy Board, Hong Kong, 13 September 1993.

Acknowledgment--Thanks are due to Dr Sophie SF Leung for critical comments on the manuscript.

References

1. National Institute of Health. Osteoporosis: Consensus Conference. JAMA 1984; 252:799-802.
2. Matkovic V. Calcium and peak bone mass. J Int Med 1992; 231:151-160.
3. British Nutrition Foundation. Non-skeletal functions of calcium in the body. In: Calcium, The report of the British Nutrition Foundation's Task Force. London: The British Nutrition Foundation, 1989:12-18.
4. British Nutrition Foundation. Plasma homeostasis, intestinal absorption and urinary excretion. In: Calcium, The report of the British Nutrition Foundation's Task Force. London: The British Nutrition Foundation, 1989:28-40.
5. Schaafsma G. Calcium in extracellular fluid: homeostasis. In: Nordin BEC, eds. Calcium in Human Biology. London: Springer-Verlag, 1988:241-259.
6. American Academy of Pediatrics. Calcium requirements in infants and childhood. Pediatr 1978, 62:826-832.
7. Leitch I & Aitken FC. The estimation of calcium requirement: a re-examination. Nutr Abs Rev 1959; 29:393-411.
8. Hsu SYC, Chan KM, Leung PC. A study of the bone mineral density of 300 Hong Kong Chinese. J Western Pacific Ortho Asson, 1987; 24(2):23-29.
9. Prentice A, Shaw A, Laskey MA et al. Bone mineral content of British and rural Gambian women aged 18-80+ years. Bone Miner 1991; 12:201-214.
10. Theintz G, Buchs B, Rizzoli R, Slosman D, Clavien H, Sizonenko PC & Bonjour JP. Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 1992; 75:1060-1065.
11. Pocock NA, Eisman JA, Hopper JL et al. Genetic determinants of bone mass in adults. J Clin Invest 1987; 80:706-710.
12. Kelly PJ, Hopper JL, Macaskill GT et al. Genetic factors in bone Turnover. J Clin Endocrin metab 1991; 72:808-813.
13. Slemenda CW, Christian JC, Williams CJ et al. Genetic determinants of bone mass in adult women: a re- evaluation of the twin model and he potential importance of gene interaction on heritability estimates. J Bone Miner Res 1991; 6:561-567.
14. Lloyd T, Rollings N, Andon MB et al. Determinants of bone density in young women, I. Relationships among pubertal development, total body bone mass, and total body bone density in premenarchal females. J Clin Endocrinol Metab 1992; 75:383-387.
15. Chan GM. Dietary calcium and bone mineral status of children and adolescents. AJDC 1991,145:631-634.
16. Turner JG, Gilchrist NL, Ayling EM, Hassall AJ, Hooke EA & Dadler WA. Factors affecting bone mineral density in high school girls. NZ Med J 1992; 105:95-96.
17. Kroger H, Kotaniemi A, Vainio P & Alhava E. Bone densitometry of the spine and femur in children by dual-energy x-ray absorptiometry. Bone Miner 1992; 17:75-85.
18. Snow-Harter C, Bouxsein ML, Lewis BT, Carter DR & Marcus R. Effects of Resistance and endurance exercise on bone mineral status of young women: a randomised exercise intervention trial. J Bone Miner Res 1992; 7:761-769.
19. Davee AM, Rosen CJ, Adler R. Exercise patterns and trabecular bone density in college women. J Bone Miner Res 1992; 5:245-250.
20. Recker RR, Davies KM, Hinders SM, Hearney RB, Stegman MR & Kimmel DB. Bone gain in young adult women. JAMA; 1992:2403-2408.
21. Jacobson PC, Beaver C, Grubb SA et al. Bone density in women: college athletes and older athletic women. J Ortho Res 1984; 2:328-332.
22. Fehily AM, Coles RJ, Evans WD & Elwood PC. Factors affecting bone density in young adults. Am J Clin Nutr 1992; 56:579-586.
23. Matkovic V, Fontana D, Tominac C et al. Factors that influence peak bone mass formation: a study of calcium balance and the inheritance of bone mass in adolescent females. Am J Clin Nutr 1990; 52:878-888.
24. Lloyd T, Andon MB, Rollings N et al. Calcium supplementation and bone mineral density in adolescent girls. JAMA 1993; 270:841-844.
25. Hu JF, Zhao XH, Jia JB, Parpia B & TC Campbell. Dietary calcium and bone density among middle-aged and elderly women in China. Am J Clin Nutr 1993; 58:219-227.
26. Metz JA, Anderson JJB & Gallagher PN. Intakes of calcium, phosphorus, and protein, and physical activity levels are related to radial bone mass in young adult women. Am J Clin Nutr 1993; 58:537-542.
27. Orwoll ES. The effects of dietary protein insufficiency and excess on skeletal health. In: Burckhardt P. Heaney RP, eds. Nutritional aspects of osteoporosis. New York: Raven, 1991:355-370.
28. Adelow BJ, Holford TR & Insogna KL. Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calif Tissue Int 1992; 50:14-18.
29. Spencer H, Kramer L, Norris C (1975). Calcium absorption and balance during high phosphorus intake in man. Fed Proc 1975; 34:888.
30. McParland BE, Goulding A, Campbell AJ. Dietary salt effects of biochemical markers of resorption and formation of bone in elderly women. Br Med J 1989; 299:834845.
31. Sabto J, Powell MJ, Breidahl MJ ,Gurr FM. Influence of urinary sodium on calcium excretion in normal individuals. Med J Australia 1984; 140:354 356.
32. Mazess RB & Barden HS. Bone density in premenopausal women: effects of age, dietary intake, physical activity, smoking and birth-control pills. Am J Clin Nutr 1991; 53:132-142.
33. Paganini-Hill, A, Chao A, Ross RK & Henderson BE. Exercise and other factors in the prevention of hip fracture: The leisure world study. Epidemiology 1991; 2:16 25.
34. Lynch SR, Berelowitz I, Seftel HC, et al. Osteoporosis in Bantu males: an interracial study. Ann New York Acad Sci 1967; 69:989-1008.
35. Luckey MM, Meier DE, Mandeli et al. Radial and vertebral bone density in white and black women: evidence for racial differences in premenopausal bone homeostasis. J Clin Endocrinol Metab 1989; 69:762-770.
36. Gilsanz V, Roe TF, Mora S. et al. Changes in vertebral bone density in black girls and white girls during childhood and puberty. New Eng J Med 1991; 325: 1597-1600.
37. McCormick DP, Ponder SW, Fawcett D, Palmer JL. Spinal bone mineral density in 335 normal and obese children and adolescents: evidence for ethnic and sex differences. J Bone Miner Res 1991; 6:507-513.
38. Garn SM, Pao EM, Rihl ME. Compact bone in Chinese and Japanese. Science 1964; 143:1439-1440.
39. Mazess RB, Cameron JR. Bone mineral content in normal US whites. In: Mazess RB. ed. International Conference on Bone Mineral Measurement. Washington DC: US Government Printing Office. 1974; 228-238. [DHEW publication (NIH) 75-683.]
40. Cummings SR, Kelsey JL, Nevitt MC, O'Dowd KJ. Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol Rev 1985; 7:178-208.
41. Ross PD, Norimatsu H, Davies JW, et al. A comparison of hip fracture incidence among native Japanese. Japanese Americans, and American Caucasians. Am J Epidemiol 1991; 133:801~09.
42. Yano K, Wasnich RD, Vogel JM, Heilbrun LK. Bone mineral measurements among middle-aged and elderly Japanese residents in Hawaii. Am J Epidemiol 1984; 119:751-764.
43. Lester GE, Anderson JJB, Tylavsky FA et al. Update on the use of distal radial bone density measurements in prediction of hip and Colle's fracture risk. J Orthop Res 1990; 8:220-226.
44. Sowers MFR, Wallace RB, Lemke JH. The relationship of bone mass and fracture history to fluoride and calcium intake: a study of three communities. Am J Clin Nutr 1986; 44:889-898.
45. Gardsell P, Johnell O, Nilsson BE. The impact of menopausal age on future fragility fracture risk. J Bone Miner Res 1991; 6:429-433.
46. Russell M, Wang J, Colt E, et al. Total body bone density (TBD) and calcium (TBCA) values for Asian vs white women matched on height, weight, age, and other bone related factors. FASEB J 1992; 6:A1944 (abstr).
47. Dempster DW & Lindsay R. Pathogenesis of osteoporosis. Lancet 1993; 341:797-801.
48. Riggs BL, Melton LJ. Involutional Osteoporosis. New Eng J Med 1986; 314:1676-1686.
49. Chan ELP, Lau E, Shek CC, MacDonald D, Woo J, Leung PC & Swaminathan R. Aged-related changes in bone density, serum parathyroid hormone, calcium absorption and other indices of bone metabolism in Chinese women. Clin Endocrin 1992; 36:375-381.
50. Peacock. Renal excretion of calcium. In: Nordin BEC, eds. Calcium in Human Biology. London: SpringerVerlag, 1988:125-170.
51. Sherman SS, Hollis BW, Tobin JD. Vitamin D status and related parameters in a healthy population: the effects of age, sex and season. J Clin Endocrinol Metab 1990; 71:405-413.
52. Halloran BP, Portale AA, Lonergan ET, Morris Jr RC. Production and metabolic clearance of 1,25-dihydroxyvitamin D in men: effect of advancing age. J Clin Endocrinol Metab 1990; 70:318.
53. Chan EPL, Lau E, Shek CC, MacDonld D, Woo J, Leung PC & Swaminathan R. Age-related changes in bone density, serum parathyroid hormone, calcium absorption and other indices of bone metabolism in Chinese women. Clin Endocrinol 1992; 36:375-381.
54. Cummings SR, Black DM, Nevitt MC et al. Bone density of various sites for prediction of hip fractures. Lancet 1993; 341:72-75.
55. Hui SL, Slemenda CW, Johnston CC. Baseline measurement of bone mass predicts fracture in white women. Ann Intern Med 1989; 111:355-361.
56. Guthrie HA. Interpretation of data on dietary intake. Nutr Rev 1989; 47(2):33-38.
57. British Nutrition Foundation. Calcium. The report of the British Nutrition Foundation's Task Force. British Nutrition Foundation, London. 1989; 83-98.
58. FAO/WHO Expert Group. Calcium requirements. FAO Nutrition Meetings Report Series No. 230. Rome: FAO, 1962.
59. Nordin BEC, Marshall DH. Dietary requirements for calcium. In: Calcium in human biology. Ed. Nordin BEC, 447-471. Springer-Verlag, London, 1988.
60. Zeegelaar EJ, Sanchez H, Luyken R, et al. Studies on physiology of nutrition in Surinam: XI The skeleton of aged people in Surinam. Am J Clin Nutr 1967; 20:43-45.
61. Chalmers J, Ho KC. Geographic variations in senile osteoporosis. The association with physical activity. J Bone Joint Surg 1970; 52B:667-75.
62. Walker ARP. The human requirement of calcium: should low intakes be supplemented? Am J Clin Nutr 1972; 25:518-530.
63. Kanis JA, Passmore R. Calcium supplementation of the diet - I. Not justified by present evidence. BMJ 1989a; 298:137-140.
64. Kanis JA, Passmore R. Calcium supplementation of the diet - II. Not justified by present evidence BMJ 1989b; 298:205-208.
65. Lee WTK, Leung SSF, Wang SF et al. Calcium supplementation in Chinese children with habitually low calcium intake. Abstracts of Joint Scientific Meeting of The Hongkong Paediatric Society and The Hongkong College of Paediatrician, Hongkong. 1993d: 05.
66. Pettifor JM, Ross P, Wang J et al. Rickets in children of rural origin in South Africa: Is low dietary calcium a factor? J Pediatr 1978; 92:320 324.
67. Eyberg CJ, Pettifor JM, Moodley G. Dietary calcium intake in rural black South African children. The relationship between calcium intake and calcium nutritional status. Hum Nutr App Nutr 1986; 40C:69-74.
68. National Research Council. Food and Nutrition Board: Recommended dietary allowances, 10th edition. Washington D.C.: National Academy Press, 1989.
69. Hegsted DM, Moscoso I, Carlos Collazos CH. A study of the minimum calcium requirements of adult. J Nutr 1952; 48:181-201.
70. Malm OJ. Calcium requirement and adaptation in adult man. Scand J Clin Lab Invest 1958;10: (Suppl 36), 108199.
71. Heaney RP, Saville PD & Recker RR Calcium absorption as a function of calcium intake. J Lab Clin Med 1975; 85:881-887.
72. Norman DA, Fordtran JS, Brinkley J et al. Jejunal and ileal adaptation to alternations in dietary calcium. J Clin Invest 1981; 67:1599-1603.
73. Norman AW. Intestinal calcium absorption: a vitamin D-hormone-mediated adaptive response. Am J Clin Nutr 1990; 51:290-300.
74. Begum A & Pereira SM. Calcium balance studies on children accustomed to low calcium intakes. Br J Nutr 1969;23: 905-911.
75. Council on Foods and Nutrition. Symposium on human calcium requirements. JAMA 1963; 185:588-593.
76. McBean LD, Speckmann EW. A recognition of the interrelationship of calcium with various dietary components. Am J Clin Nutr 1974; 603-609.
77. Eastell R, Vieira NE, Yergey AL & Riggs L (1989). One-day test using stable isotopes to measure true fractional calcium absorption. J Bone Miner Res 1989; 4:463-468.
78. DeGrazia JA, Ivanovich P, Fellows H et al. A double label technique for measurement of intestinal absorption of calcium in man. J Lab Clin Med 1965; 66:822-829.
79. Allen LH. Calcium bioavailability and absorption: a review. Am J Clin Nutr 1982; 35:783-808.
80. Anand CR, Linkswiler HM. Effect of protein intake on calcium balance of young men given 500 mg calcium daily. J Nutr 1974; 104:695.
81. Sabto J, Powell MJ, Breidahl MJ ,Gurr FM. Influence of urinary sodium on calcium excretion in normal individuals. Med J Australia 1984; 140:354-356.
82. Department of Health. Dietary reference values for food energy and nutrients for the United Kingdom. Report on Health and Social subjects 41. London: H.M. Stationery Office, 1991.
83. Smith KT, Heaney RP, Flora L & Hinders SM Calcium absorption from calcium citrate-malate. Calcif Tissue Int 1987; 41:351-352.
84. Miller JZ, Smith DL, Flora L et al. Calcium absorption from calcium carbonate and a new form of calcium (CCM) in healthy male and female adolescents. Am J Clin Nutr 1988; 48:1291-1294.
85. Lee WTK, Leung SSF, Fairweather-tait S et al. True calcium absorption in relation to calcium intake in Chinese children. Abstracts of Joint Scientific Meeting of The Hongkong Paediatric Society and The Hongkong College of Paediatrician, Hongkong. 1993c: P13.
86. Nicholls L & Nimalasuriya A. Adaptation to a low calcium intake in reference to the calcium requirements of a tropical population. J Nutr 1939; 18:563-577.
87. Chinese Nutrition Society. Recommended Dietary Allowances. Acta Nutrimenta Sinica 1990; 12:10.
88. Matkovic V, Kostial K, Simonovic I et al. Bone status and fracture rates in two regions of Yogoslavia. Am J Clin Nutr 1979; 32:540-549.
89. Yano K, Heilbrun LK, Wasnich RD et al. The relationship between diet and bone mineral content of multiple sites in elderly Japanese-American men and women living in Hawaii. Am J Clin Nutr 1985; 42:877 888.
90. Halioua L & Anderson JJB. Lifetime calcium intake and physical activity habits: independent and combined effects on the radial bone of healthy premenopausal Caucasian women. Am J Clin Nutr 1989; 49:534-541.
91. Hu JF, Zhao XH et al. Bone density of pre- and postmenopausal Chinese women consuming diets high, moderate or lacking in dairy products. In: Abstracts of 'Diet in prevention and treatment of chronic disease' Conference. Seattle, 1991:20.
92. Lee WTK, Leung SSF, Lui SSH & Lau J. Relationship between long term calcium intake and bone mineral content of children aged from birth to 5 years. Bri J Nutr 1993; 70:235-248.
93. Lee WTK, Leung SSF, Ng MY et al. Bone mineral content of two populations of Chinese children with different calcium intakes. Bone Miner 1993; 23:195-206.
94. Kelly PJ, Pocock NA, Sambrook PN, Eisman JA. Dietary calcium, sex hormone, and bone mineral density in men. BMJ 1990; 300:1361-1364.
95. Johnston CC, Miller JZ, Slemenda CW et al. Calcium supplementation and increases in bone mineral density in children. New Eng J Med 1992; 327:82-87.
96. Anderson JJB, Tylavsky FA, Lacey JM, Talmage RV. Black-white differences in bone status of young women according to calcium intake. In: Cohn DV, Martin TJ, meunier PJ. Calcium regulation and bone metabolism. Vol. 9, Amsterdam: Excerpta Medica, 1987; 696 (abs).
97. Reid IR, Mackie M, Ibbertson HK. Bone mineral content in Polynesian and white New Zealand women. BMJ [Clin Res] 1986; 292:1547-1548.
98. De Schepper J, Derde MP, Van den Broeck M., Pipsz A, Jonckheer MH. Normative data for lumbar spine bone mineral content in children: influence of age, height, weight, and pubertal stage. J Nucl Med 1991; 32:216-220.
99. Katzman DK, Bachrach LK, Carter DR & Marcus R. Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab 1991; 73:1332-1339.
100. Bonjour JP, Theintz G, Buchs B, Slosman D & Rizzoli R. Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab 1991; 73:555-563.
101. Snedeker SM, Smith SA, Greger JL. Effect of dietary calcium and phosphorus levels on the utilisation of iron, copper, and zinc by adult males. J Nutri 1982; 112:136143.
102. Dawson-Huges B, Seligson FH, Huges VA. Effects of calcium carbonate and hydroxyapatite on zinc and iron retention in postmenopausal women. Am J Clin Nutri 1986; 44:83-88.
103. Robertson WG. Dietary factors important in calcium stone formation. In: Schwille, Smith, Robertson & Vahlensieck (ed. ) . Urolithiasis and related clinical research. 61-68. Plenum Press, New York, 1985.
104. Heaney RP, Weaver CM, Recker RR. Calcium absorbability from spinach. Am J Clin Nutr 1988; 47:707-709.
105. Heaney RP, Weaver CM. Oxalate: effect on calcium absorbability. Am J Clin Nutr 1989; 50:830-32.
106. Heaney RP, Weaver CM. Calcium absorption from kale. Am J Clin Nutr 1990; 51:656-657.
107. Heaney RP, Weaver CM, Fitzsimmons ML. Soybean phytate content: effect on calcium absorption. Am J Clin Nutr 1991; 53:745-747.

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