Chapter 23 Minerals: Calcium KARIN PIEHL AULIN Introduction Calcium is a micronutrient with great importance to many cellular events in different tissues in the body, as well as forming the major structural component of bone. Athletes are often concerned that their normal diet will not provide sufﬁcient micronutrients, and the need for an adequate dietary intake of calcium is as much a concern for athletes as it is for the general population. Augmentation of the diet with speciﬁc calcium supplements and with calcium-enriched foods is common practice among athletes and non-athletes alike, but there is limited information as to whether the need for calcium is increased by physical activity, and whether such supplementation is warranted. The US Surgeon General’s Report (1988) states that ‘inadequate dietary calcium consumption in the ﬁrst three to four decades of life may be associated with increased risk for osteoporosis in later life due to a low peak bone mass’. Osteoporosis is a chronic disease characterized by a progressive loss of bone mass: it affects women more than men, partly because of the role played by a falling oestrogen level after the menopause. Bone loss is widely accepted as a normal part of the ageing process, and occurs at a rate of about 0.5–1.0% per annum after the age of 40 (Cohn et al. 1976): by age 90, one third of women and one sixth of men will have suffered hip fractures as a consequence. However, a number of nutritional and lifestyle factors have a major impact on the rate of mineral loss from the skeleton: 318 these factors can be important in slowing this process, and thus in delaying the point at which the bone mineral density becomes so low that the fracture threshold is easily exceeded. Other important factors reported to be associated with the maintenance of bone health are an adequate level of physical activity and avoidance or cessation of cigarette smoking and excess alcohol intake. However, while there is a clear role for physical activity in maintaining bone mass, very high levels of exercise in women have been associated with some degree of bone loss (Drinkwater et al. 1990), so there are clearly a number of issues of importance for women, and perhaps also to a lesser extent for men, involved in sports where high training loads are involved. Roles of calcium in the body Calcium is an essential nutrient and a major component of mineralized tissue and is the mineral found in the largest quantity in the body, representing about 1.5–2% of body mass in the average adult: for men, total body calcium content is about 1000–1100 g, and for women, about 800 g (Cohn et al. 1976). Approximately 99% of the total body calcium is located in the bones. The remaining 1% is accounted for by the calcium found in the blood, muscle and nervous tissue where calcium is necessary for blood coagulation, muscle contraction and nerve conduction: although the amounts are small, the role of calcium is crucial for normal functioning. minerals: calcium Bone matrix is a mixture of tough ﬁbres (made of type I collagen), which resist pulling forces, and solid particles (calcium phosphate as hydroxyapatite crystals), which resist compression. Bone is by no means a permanent and immutable tissue. There is a continuous turnover and remodelling of the matrix with a concomitant release and uptake of calcium: the cells involved in bone breakdown are osteoclasts, while the osteoblasts are involved in bone formation. The regulators of calcium metabolism in bone tissue are two hormones, parathyroid hormone (PTH) and calcitonin. Excess PTH results in a rise in the blood calcium with a corresponding fall in the calcium content of the bones, and a loss of calcium from the body by increased excretion in the urine. PTH, and exposure to sunlight, also stimulates the formation of the active form of vitamin D, which governs the absorption of calcium from the small intestine. The ability to regulate the uptake of calcium is important, and differences in bone mineral density can be demonstrated in response to exercise, even between groups with the same dietary calcium intake. Calcitonin is released when plasma calcium increases and stimulates bone formation. Calcium is excreted by the large intestine and, to a lesser extent, by the kidney and by the dermis. In the overall function of skeletal muscle, calcium plays two essential regulatory roles. First, calcium is the link between excitation and contraction. The concentration of free calcium in the cytosol is low (about 10–8 m) in resting muscle (Martonosi & Beeler 1983), whereas its concentration in the extracellular ﬂuid and in the endoplasmic reticulum (ER) is high. Calcium is involved in a series of events which converts the electrical signal of the action potential arriving at the synaptic terminal into a chemical signal that travels across the synapse where it is converted back into an electrical signal in the postsynaptic cell. Release of calcium from the terminal cisternae of the sarcoplasmic reticulum in response to membrane depolarization upon the arrival of an action potential allows the actin and myosin ﬁlaments to interact. The plasma membrane and the 319 ER membrane have mechanisms to regulate the calcium concentration gradient during resting conditions and to restore it after muscle and nerve cell stimulation (Alberts et al. 1994). The activation process involves the binding of calcium to troponin C, one of the regulatory proteins associated with the actin ﬁlaments, and the change in shape of these proteins allows interaction between actin and myosin to occur. Calcium is then pumped back into the terminal cisternae by an energy-dependent transporter in a process that consumes adenosine triphosphate (ATP), allowing relaxation of the muscle to occur. There is good evidence that fatigue during highintensity exercise may involve a disruption of the cell’s calcium-handling capability (Maughan et al. 1997). A number of substances, including caffeine, can alter the response of the muscle to a single action potential, and the effects of some of these compounds on exercise capacity may be mediated by effects on calcium transport. These processes are described in detail by Jones and Round (1990). A second key process requiring calcium is the activation of numerous cellular enzymes involved in energy production, and calcium is important to both glycogenolysis and the glycolytic pathway in generating ATP (Tate et al. 1991; Clarkson & Haymes 1995). It seems sensible that the same process that allows the muscle to do work is involved in the regulation of ATP provision. The activity of phosphorylase, the key enzyme involved in glycogen breakdown, is stimulated by increasing cytosolic calcium concentration (Maughan et al. 1997) and this is important for the activation of the glycolytic pathway at the onset of exercise. Calcium intake An adequate calcium intake is needed to achieve optimal peak bone mass in the ﬁrst two or three decades of life, to maintain bone mass throughout the middle years of life, and to minimize bone loss in the later years (Andersson 1996). A daily calcium intake that is sufﬁcient to meet the requirement may be achieved through diet alone, 320 nutrition and exercise if some attention is paid to the composition of the diet. Alternatively, calcium-fortiﬁed food or calcium supplementation may be employed to meet the need. The amount of calcium available from the diet depends on the total dietary calcium intake, the bioavailability, which depends in turn on the amount of calcium in solution and on the presence of other dietary components, and on the activity of the intestinal calcium transport systems. The bioavailability is inﬂuenced by the presence of anions that form insoluble compounds that cannot be absorbed: these include oxalate (which is present in rhubarb and spinach) and polyphosphate. Vitamin D status will determine the activity of the calcium transporters in the intestine. All of these factors, in addition to the ongoing losses of calcium from the body, will inﬂuence the amount of calcium that the diet must supply to meet the individual’s requirement. When body mass is taken into account, growing children require as much as two to four times as much calcium as adults, and the United States recommended dietary allowance (RDA) for calcium is greatest during adolescence (11–18 years) and early adulthood (19–24 years), being in the order of 1200 mg · day–1 (National Research Council 1989). Males and females of all ages have the same calcium requirement except when females are pregnant or lactating. The RDA for children (1–10 years) and adults 25 years and older is 800 mg · day–1. The National Academy of Science Food and Nutrition Board recently suggested new guidelines for calcium intake. They recommend: during early childhood (1–3 years) 500 mg · day–1, 800 mg · day–1 between 4 and 8 years, 1300 mg · day–1 during adolescence (9–18 years) and 1000 mg · day–1 between the ages of 18 and 50 years. In the general US population, it is estimated that the average dietary calcium intake of men is about 115% of the 1989 RDA, but for women the ﬁgure is only 78%: for children, it is estimated that the mean intake is about 105% of the RDA (US Surgeon General 1988). Corresponding ﬁgures for the UK indicate rather similar values, with a daily mean intake of 940 mg for men and 717 mg for women (Gregory et al. 1990). However, as the RDA for calcium in the UK is only 500 mg for men and for women, the average intake was well above the RDA. This discrepancy between countries in recommendations for dietary intake reﬂects the uncertainty as to requirements: the dietary intake necessary to maintain calcium balance has been reported to be anything between 200 mg · day–1 and over 1000 mg · day–1 (Irwin & Kienholz 1973). The high value recommended for the American population greatly exceeds the desirable intake recommended by the WHO/FAO, and reﬂects the high dietary content of protein and phosphate in that country: both protein and phosphate are reported to increase calcium loss. Surveys of dietary habits in female adolescent athletes (gymnasts, ballet dancers and distance runners) show their average calcium intake to be well below RDA and often related to their lowenergy intake in order to maintain a low body weight (Carroll et al. 1983). Low energy intake together with a high weekly training load will lead to a decreased percentage of body fat, and insufﬁcient levels of circulating oestrogen, resulting in menstrual dysfunctions such as oligomenorrhea or amenorrhea (Drinkwater et al. 1984, 1990). Several cross-sectional studies have shown signiﬁcant relationships between body mass and bone mineral density and between body mass and susceptibility to osteoporotic fracture (Sowers et al. 1991; Lindsay et al. 1992). Restriction of energy intake (which resulted in a 5% reduction in dietary calcium intake) for a period as short as 6 months has been shown to result in a signiﬁcant reduction in bone mineral density in healthy young women, even though there was only a moderate (3.4 kg) loss of body mass in these subjects (Ramsdale & Bassey 1994). The combination of low body mass, low circulating oestrogen levels and low dietary calcium intake clearly creates a high risk situation for development of early osteoporosis, and the possibility of stress fractures due to overload of bone tissue will then increase. Resumption of menses by regain in body weight may restore some of the lost bone tissue but not all is likely to be regained, minerals: calcium depending on the persistence of the amenorrhoea (Drinkwater et al. 1986). Foods rich in calcium include dairy products, some canned ﬁsh (especially if eaten with bones), some vegetables, including broccoli, spinach and collard greens, tofu, and some calcium-enriched grain products. UK data for the general population indicate that milk and milk products provided about one half of the total calcium intake, while cereal products provided about 25%: vegetables contributed only about 7%, and the use of supplements was negligible (Gregory et al. 1990). Where energy intake is a concern, as in weight category sports, or when energy intake is otherwise restricted, the use of reduced-fat dairy products should be encouraged: a wide range of low to moderate fat varieties can be used to add variety to the diet. Calcium has been reported to inhibit the absorption of iron from the food and it is therefore suggested that these two nutrients should not be taken together in large amounts (Gleerup et al. 1995). When both iron status and calcium status are precarious, special attention must be paid to the initiation of any supplementation regimen. This may be particularly relevant to female athletes, who may suffer from anaemia due to both low energy intake and loss of iron through the menses. Calcium balance Whole body net calcium balance reﬂects the relationship between the dietary calcium intake and all routes of calcium loss. Positive calcium balance occurs when calcium intake exceeds calcium loss, and is necessary for bone growth and peak bone mass to be achieved. Negative calcium balance will lead to a decrease in bone mass and density. Calcium loss is the sum of the faecal, urinary, and dermal calcium losses. Faecal calcium loss accounts for about 75–80% of the dietary calcium ingested (Schroeder et al. 1972), but about 20% of this is of endogenous origin (Melvin et al. 1970). As discussed further below, the urinary calcium loss may be inﬂuenced by a number of factors, and the acidity of the urine, 321 which may in turn be inﬂuenced by the composition of the diet, appears to be an important factor (Ball & Maughan 1997). The loss of calcium through the skin is often estimated at 60 mg · day–1, but this may substantially underestimate the actual calcium loss of individuals who engaged in strenuous training programmes (Matkovic 1991). Sweat calcium losses as high as 57 mg · h–1 have been reported during exercise (Krebs et al. 1988). Sweat calcium concentration is typically about 1 mmol · l–1 (40 mg · l–1), so losses may be very much greater than this when sweat rates are high or when prolonged exercise is performed, especially in hot environments (Shirreffs & Maughan 1997). Dietary factors other than calcium intake may be of importance, and the association between high protein diets and an increased urinary calcium loss is widely accepted (Lutz 1984; Kerstetter & Allen 1990); this effect appears to be a consequence of the acid load that results from protein metabolism. The effects of an acid load in increasing urinary calcium output are well established, and the US Surgeon General’s Report on Nutrition and Health (1988) concluded that ‘increased acidity induces calcium loss by increasing renal excretion directly as well as by increasing the dissolution of mineral from the skeleton and impairing mineral deposition.’ A recent comparison of the dietary intake of omnivorous women and a matched group of vegetarians showed that the vegetarians had a lower dietary protein intake and a lower 24-h total urinary acid excretion than the omnivorous women (Ball & Maughan 1997). Although there were no differences between these groups in the estimated (7-day weighed intake) dietary calcium intake, the daily urinary calcium excretion of the omnivores was signiﬁcantly higher than that of the vegetarians. These results are consistent with the suggestion that the acid/ alkaline characteristics of the habitual diet have implications for calcium balance, and that this may be amenable to manipulation by alteration of speciﬁc dietary components. There have been numerous recent reviews of the current state of knowledge regarding nutri- 322 nutrition and exercise Fig. 23.1 Most forms of exercise are good for bone health and should be encouraged in youngsters. Only a few athletes, most commonly young women in sports where low body mass confers an advantage, are likely to suffer accelerated bone mass. Photo © Allsport / M. Powell. tion and bone metabolism and these have been summarized in the US Surgeon General’s Report on Nutrition and Health (1988) (see Chapter 7). Exercise and calcium balance Acute exercise results in a prompt increase in serum calcium, both in its ionized and nonionized forms. This may be due in part to lactic acidosis rather than to changes in PTH and calcitonin concentrations, and haemoconcentration is also likely to be a signiﬁcant factor (Vora et al. 1983; Cunningham et al. 1985). Marathon running was found to be accompanied by a transient decrease in urinary calcium and serum osteocalcin levels (Malm et al. 1992). Endurance training has been reported to be associated with increased serum levels of the active form of vitamin D, leading to increased calcium absorption and a rise in total body calcium (Yeh & Aloia 1990). A few studies have demonstrated exerciserelated elevations in PTH (Ljunghall et al. 1985, 1986; Salvesen et al. 1994), but this has not been conﬁrmed in other studies (Aloia et al. 1985). The inﬂuence of calcium intake and physical activity on peak bone mass has been the subject of much attention (Kanders et al. 1988; Mazess & Barden 1991; Recker et al. 1992). There are both cross-sectional and longitudinal studies that favour a beneﬁcial effect of calcium on the adult skeleton and there are others that ﬁnd no relationship between dietary calcium and bone mass and rate of bone loss. Peak bone mass is achieved during the third decade of life. Apart from calcium intake, heredity is also an important factor determining peak bone mass. A study on identical twins, where one twin in each pair received calcium supplementation and the other a placebo, suggested that extra calcium in the diet is beneﬁcial to the achievement of peak bone mass prior to puberty (Johnston et al. 1992). The role of physical activity in optimizing bone growth as well as maintaining bone mass is well established (Torgerson et al. 1995): acute reductions in weight-bearing activity are associated with a dramatic loss of calcium. Measurements of prolonged bed rest in healthy volunteers and in patients, as well as in astronauts subjected to microgravity, have all shown an increased calcium loss and a reduced skeletal mass (Anonymous 1983). Increased physical activity, and in particular running, has been shown to be associated with an increased bone density (Lane et al. 1986), and it seems clear that the physical stress imposed on the bone is an important factor (Lanyon 1992; Wolman 1994). This is supported by a recent study showing increases in bone area in adult male rats subjected to a resistance training programme (Westerlind et al. 1998). There is, however, little information on the type, frequency, duration and intensity of exercise that will optimize bone mass and minimize the age-related loss. minerals: calcium Apart from the implications for the development of osteoporosis in later life, a low bone density may be detrimental in athletes. Myburgh et al. (1990) found that athletes with lower extremity stress fractures had signiﬁcantly lower femoral and lumbar mineral densities than matched athletic control subjects. Athletes with stress fractures had signiﬁcantly lower calcium intakes and had lower intakes of dairy products. Injured female athletes were more likely to have irregular menstrual cycles and less likely to use oral contraceptives. This was not conﬁrmed among female ballet dancers but a great number of dancers with stress fractures avoided dairy products (Frusztajer et al. 1990). A lifetime history of calcium intakes exceeding 800 mg · day–1 appears to reduce the risk for hip fractures in older women compared with women with lower calcium intake (< 450 mg · day–1) and this also seems to hold for men (Matkovic et al. 1979). Milk consumption during childhood and adolescence and as an adult was associated with a greater bone mass in postmenopausal women, but total calcium intake was not associated with bone mass (Sandler et al. 1985; Bauer et al. 1993). Exercise appears to be more important in preventing trabecular bone loss while calcium intake may be a more important inﬂuence on cortical bone loss. Conclusion Intake of sufﬁcient amounts of energy to balance the expenditure, maintenance of circulating hormone levels, and regular participation in some form of weight-bearing exercise are of greatest importance to achieve and preserve skeletal health. This is important for the avoidance of stress fractures in young athletes and for the preservation of bone health in later life. An adequate dietary intake of calcium is also essential, and this can be achieved by consumption of dairy products (which may be reduced-fat varieties) and other foods rich in calcium. 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