Dietary calcium intake is most often considered in terms of promoting bone health. In fact, the recommendations for dietary calcium intake established by the National Institutes of Health (NIH), National Academy of Sciences (NAS), and the United States Department of Agriculture (USDA) have been made with the specific aim of preventing osteoporosis [1••]. The NIH defines osteoporosis as a disease characterized by low bone mass and structural deterioration of bone tissue, leading to bone fragility and an increased susceptibility to fractures of the hip, spine, and wrist . Calcium is integral in bone remodeling; that is, the constant process of bone formation and bone resorption. Whether the objective is to maximize attainment of peak bone mass (PBM) during childhood and early adulthood, or to prevent bone loss with advancing age, dietary calcium intake is a key factor . In the United States, it is estimated that calcium intakes for children and adults fall below the recommended minimums, and this is especially evident in the elderly, who are at greatest risk for osteoporosis . However, the role of calcium in the body is not limited to the parameters of bone health. It also includes muscle contraction and subsequently heart beat regulation, nerve impulse conduction, regulation of blood pressure and water balance, and a myriad of other functions such as cell division, immune function, energy and fat metabolism, and the transport of nutrients and other substances across cell membranes . Athletes require special attention with regard to calcium needs and adequate dietary calcium intake. Although promoting bone health and preventing osteoporosis is very important for this particular group, there are even further considerations for dietary calcium intake for athletes. Factors such as weight-bearing exercise, electrolytes lost via sweat, and the female athlete triad must be considered in relation to calcium needs and dietary calcium intake.
Two factors determine adult bone health. One is the maximum attainment of PBM achieved during periods of growth and concluding during early adulthood . Peak bone mass is defined as the maximum amount of bone mass achieved during skeletal growth. Second is the rate at which bone is lost during advancing age, with special concern afforded to women during the menopausal years. It is estimated that bone loss averages approximately 2% to 3% of total bone mass over the 5 to 10 years following the onset of menopause .
Physical activity has been deemed the primary modifiable stimulus that affects bone growth and development in adolescents and young adults [1••]. Regular physical activity improves bone mineral status, also known as bone mineral density (BMD) by way of mechanical stresses on bone structures . Specifically, high-impact sports (eg, volleyball, basketball) result in the greatest markers of bone formation as well as the highest BMD at weight-bearing sites, such as the lumbar spine and the femoral neck [3,8]. Conversely, low- or nonimpact sports such as swimming have negative effects on BMD .
Dietary calcium intake also promotes bone health. During infancy and adolescence, there is an increased need for calcium intake and a higher rate of calcium absorption compared with any other age group . It is imperative that calcium intake is adequate during this time to establish healthy bones. For women, attainment of PBM in their late 20s is a critical factor in the prevention or minimization of the risk of osteoporosis associated with aging [10••]. Female athletes who restrict energy intake to the point of incurring menstrual dysfunction have been shown to underachieve PBM, and thus have an increased risk for developing osteoporosis .
Micronutrient Needs for Physical Activity
Athletes are exposed to physiologic stressors and circumstances above and beyond those of sedentary individuals. Regular, intense physical training may increase the athlete's need for vitamins and minerals above the standard recommendations due to the following factors: decreased gastrointestinal absorption, increased sweat losses, losses incurred via urine and feces, and increased needs associated with tissue maintenance and repair [10••,11]. Those athletes who are at greatest risk for micronutrient deficiencies are those who restrict overall intake, employ drastic measures for weight loss, eliminate one or more food groups from their diet, or consume foods that are not nutrient dense in an attempt to restrict caloric intake . Exercise capacity may be impaired and performance may suffer for those athletes who do not have an adequate intake of micronutrients in their diet . Deficiencies that often parallel dietary calcium deficiency include energy, protein, and vitamin D, all of which, when deficient, can negatively affect bone health [10••]. Exercise and the elevated metabolism associated with exercise itself does not increase the body's need for dietary calcium; however, electrolytes are oftentimes lost in high volume due to sweat concentration and dietary calcium intake may need to be augmented to compensate for those losses and to prevent deficits from occurring [10••].
Female Athlete Triad
One major consideration for female athletes in terms of calcium needs and supplementation is the female athlete triad. This consists of three conditions: disordered eating, amenorrhea, and osteoporosis . Physically active women may fail to meet energy needs during training by intentionally restricting intake, or failing to replenish energy intake with respect to energy output associated with training, purging, or compulsive exercise. Food restriction and purging can result in irreversible bone loss, as well as fluid and electrolyte imbalances [15•]. Menstrual dysfunction, specifically amenorrhea, causes hypoestrogenism, which is linked with osteoporosis [16,17]. Weight gain and the resumption of menses can result in an increased BMD [18,19]. Amenorrheic athletes should increase their calcium intake to a minimum of 1500 mg/d, exceeding the standing recommendation of 1200 mg/d for healthy, menstruating adolescents [15•].
The dietary reference intake (DRI) is used as a standard for recommended dietary calcium intake is known as adequate intake (AI). The AI is based on estimates of nutrient intake by a group of healthy people that is assumed to be adequate . There is not enough data available to establish a recommended dietary allowance (RDA) or estimated average requirement for calcium and therefore the AI is set at a level that is proposed to meet or exceed the needs of almost all members of a group . There is a tolerable upper intake level for calcium that indicates the highest daily average intake of this mineral without posing adverse health affects. Optimal calcium intake is 1200 mg/d for teenagers and young adults, 1000 mg/d for women ages 25 to 50 years, and 1500 mg/d for postmenopausal women who are not on estrogen replacement therapy . As previously stated, another subgroup that has increased calcium needs is ammenorrheic athletes, who require at least 1500 mg/d of dietary calcium [15•]. Adults over the age of 50 require 1200 mg/d [21••]. Table 1 details the recommended dietary calcium intakes by age group.
Calcium Sources in the Diet
The American College of Sports Medicine, American Dietetic Association, and Dietitians of Canada encourage athletes “to strive to consume diets that provide at least the RDA or DRI for all micronutrients from food” . Dairy products and other high calcium content foods are referred to as “preferred” calcium sources as opposed to commercial calcium supplements [22–25]. Seventy percent of the calcium intake in the diet comes from milk and dairy products . The primary source of dietary calcium is cheese, followed by milk, milk products and yogurt . However, dairy products are not the only sources of dietary calcium. Kale and turnip greens, broccoli, tofu, and calcium-fortified foods such as orange juice are all examples of foods that contribute to overall dietary calcium intake. Table 2 provides a list of various foods and their calcium contents.
Factors that Influence Calcium Absorption
The amount of calcium an individual consumes is only one consideration in terms of calcium utilization and incorporation into bone. Certain foods increase the likelihood that calcium will be absorbed into bone, whereas others actually hinder calcium absorption by forming insoluble compounds or promote calcium excretion in the urine . Both phosphorus and vitamin D are effective in enhancing calcium uptake and incorporation in bone. The majority of Americans do not obtain adequate levels of vitamin D, especially older adults and the elderly . Phosphorus intake is a critical factor with regard to promoting the incorporation of absorbed calcium in bone, but excessive phosphorus intake can lead to a decrease in the production of the metabolically active form of vitamin D, 1,25 dihydroxyvitamin D, which may adversely affect bone metabolism [1••,28]. A calcium to phosphorus ratio of 2:1 is necessary for bone production . Those substances that form insoluble compounds with calcium include phytates, which are found in bran and most cereals, oxalates in spinach, rhubarb, and walnuts, and tannins in tea [1••,26]. This causes special concern for vegans or strict vegetarians who either completely eliminate or severely restrict dairy products in their diets and rely on nonanimal food sources for their calcium intake. A note should also be made that soy products also contain high levels of phytates. Increasing dietary protein intake, especially animal proteins, is associated with increased urinary calcium losses and is especially detrimental to bone health when dietary calcium intakes are also inadequate [1••,30]. Sodium intake is another potential factor that affects calcium excretion in the urine. Both sodium and calcium compete for resorption in the renal tubules. Nordin et al.  report that for every 2300 mg of sodium excreted by the kidney, approximately 40 to 60 mg of calcium are also lost. Potassium, which is found primarily in plant protein foods such as legumes and grains, in high levels of intake will decrease urinary calcium excretion .
Calcium supplementation is thought to slow age-related bone loss and reduce the risk of fracture at vulnerable sites in middle aged men and women . Calcium supplements are among the most widely prescribed dietary supplements. There are several types of calcium supplements and each calcium salt carries with it a distinct absorption rate as follows: calcium carbonate, 36% to 42% is absorbed; calcium acetate and calcium lactate, 28% to 36% is absorbed; calcium citrate, 27% to 33% is absorbed; calcium gluconate, 24% to 30% is absorbed, and calcium lactate, 28% to 36% is absorbed . In other studies, it has been demonstrated that calcium citrate and calcium carbonate are equal with regard to the bioavailability of calcium . Table 3 lists various calcium supplements and their calcium content. Taking calcium carbonate as divided doses with meals can help to minimize side effects such as gas, bloating, and constipation, and improve absorption . Those individuals with decreased gastric acid production (eg, the elderly) may experience a decrease in the absorption of calcium from supplements unless that supplement is taken with food. Caution should be given with regard to calcium from bone meal, dolomite, and oyster shells as these have historically contained high levels of lead and cadmium, which can be toxic .
Dietary calcium intake is a key factor in promoting bone health and preventing osteoporosis. In addition to osteoporosis prevention, athletes must also consider the effect of weight-bearing exercise with regard to skeletal health, calcium losses associated with sweating, and disorders such as the female athlete triad. Calcium needs are highest during childhood and adolescence, at which time bone formation and development is critical. Other groups that require a higher intake of dietary calcium are the elderly, specifically postmenopausal women who are not taking hormone replacement therapy, and amennorheic athletes. Increased physical activity in and of itself does not increase the need for dietary calcium intake. Oftentimes when athletes restrict overall energy intake, they inherently restrict intakes of calcium and other important nutrients like vitamin D. When dietary calcium intake is adequate to meet needs, attention must be given to the factors that may either promote or inhibit the uptake and utilization of the ingested calcium. In the event that adequate dietary calcium cannot be met with diet alone, calcium supplements may be useful to compensate for the deficit.
References and Recommended Reading
Papers of particular interest, published recently, have been highlighted as: • Of importance, •• Of major importance
1.•• Lanou AJ, Berkow SE, Barnard ND: Calcium, dairy products, and bone health in children and young adults: a reevaluation of the evidence.Pediatrics
A very comprehensive review of the literature from 58 studies, including cross-sectional, retrospective, and prospective studies, and randomized control trials.
2. National Institutes of Health: Osteoporosis and Related Bone Diseases National Resource Center.
3. New SA: Exercise, bone and nutrition.Proc Nutr Soc
4. Looker AC, Loria CM, Carroll MD, et al.
: Calcium intakes of Mexican Americans, Cubans, Puerto Ricans, non-Hispanic whites, and non-Hispanic blacks in the United States.J Am Diet Assoc
5. Weaver C, Heaney RP: Calcium.Modern Nutrition in Health and Disease.
Edited by Shils ME, Olson JA, Shike M, Ross AC. Philadelphia: Lippincott, Williams and Wilkins; 1999:141–156.
6. Cooper C: Epidemiology of osteoporosis.Osteoporos Int
7. Guezennec CY, Chalabi H, Bernard J, et al.
: Is there a relationship between physical activity and dietary calcium intake? A survey in 10, 373 young French subjects.Med Sci Sports Exerc
8. Creighton DL, Morgan AL, Boardley D, Brolinson PG: Weight-bearing exercise and markers of bone turnover in female athletes.J Appl Physiol
9. Peacock M: Calcium absorption efficiency and calcium requirements in children and adolescents.Am J Clin Nutr
10.•• Petrie HJ, Stover EA, Horswill CA: Nutritional concerns for the child and adolescent competitor.Nutrition
Comprehensive recommendations for young athletes in terms of macronutrient, micronutrient intake, and fluid intake, as well as addressing specific nutrition-related issues with this population.
11. Campbell WW, Geik RA: Nutritional concerns for the older athlete.Nutrition
12. American College of Sports Medicine, American Dietetics Association, Dietitians of Canada: Joint position statement. Nutrition and athletic performance.Med Sci Sports Exerc
13. Maughan RJ: Role of micronutrients in sport and physical activity.Br Med Bull
14. Yeager KK, Agostini R, Nattiv A, Drinkwater B: The female athlete triad: disordered eating, amenorrhea, osteoporosis.Med Sci Sports Exerc
15.• Committee on Sports Medicine and Fitness: Medical concerns in the female athlete.Pediatrics
Provides a detailed review of the female athlete triad and the consequences of menstrual dysfunction, hormone imbalance, and disordered eating for female athletes.
16. Cann CE, Genant HK, Ettinger B, Gordon GS: Spinal mineral loss in oophorectomized women: determination by quantitative computed tomography.JAMA
17. Cann CE, Martin MC, Genant HK, Jaffe RB: Decreased spinal mineral content in amenorrheic women.JAMA
18. Dhuper S, Warren MP, Brooks-Gunn J, Fox R: Effects of hormonal status on bone density in adolescent girls.J Clin Endocrinol Metab
19. Bachrach LK, Katzman DK, Litt IF, et al.
: Recovery from osteopenia in adolescent girls with anorexia nervosa.J Clin Endocrinol Metab
20. Barr SI, Murphy SP, Poos MI: Interpreting and using the Dietary Reference Intakes in dietary assessment of individuals and groups.J Am Diet Assoc
21.•• Campbell WW, Geik RA: Nutritional considerations for the older athlete.Nutrition
Review article discussing the nutritional needs and concerns of older athletes, an oftentimes overlooked population.
22. National Institutes of Health: Consensus Development Conference Statement. Osteoporosis Prevention, Diagnosis, and Therapy.
Bethesda MD: National Institutes of Health; 2000:27–29.
23. National Institutes of Health: Consensus development panel on optimal calcium intake. NIH Consensus conference: optimal calcium intake.JAMA
24. Institute of Medicine: Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride. Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board.
Washington, DC: National Academy Press; 1997.
25. US Department of Agriculture and US Department of Health and Human Services: Nutrition and Your Health: Dietary Guidelines for Americans.
Washington, DC: US Department of Agriculture and US Department of Health and Human Services; 2000.
26. Gueguen L, Pointillart A: The bioavailability of dietary calcium.J Am Coll Nutr
27. Moore C, Murphy MM, Keast DR, Holick MF: Vitamin D intake in the United States.J Am Diet Assoc
28. Groff JL, Gropper SS: Advanced Nutrition and Human Metabolism.
Belmont, CA: Wadsworth Thompson Learning; 2000.
29. Kass-Wolff JH: Calcium in women: healthy bones and much more.JOGNN
30. Massey LK: Dietary animal and plant protein and human bone health: a whole foods approach.J Nutr
31. Nordin BE, Need AG, Morris HA, Horowitz M: The nature and significance of the relationship between urinary sodium and urinary calcium in women.J Nutr
32. Heaney RP, Dowell MS, Bierman J, et al.
: Absorbability and cost effectiveness in calcium supplementation.J Am Coll Nutr
33. Blanchard J, Aeschlimann JM: Calcium absorption in man: some dosing recommendations.J Pharmacokinet Biopharm
34. National Osteoporosis Foundation: Calcium supplements.