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Patient involvement No patients were involved in setting the research question or the outcome measures, nor were they involved in the design and implementation of the study. Results Baseline characteristics We identified 59 randomised controlled trials of calcium intake that reported BMD as an outcome. View this table: View popup View inline. Subgroup analyses We carried out additional subgroup analyses when there were 10 or more trials in an analysis and three or more trials in each subgroup.

Discussion Principal findings Increasing calcium intake from dietary sources slightly increased bone mineral density BMD by 0. Strengths and limitations of the study The strength of this meta-analysis is its comprehensive nature. Implications of findings The absence of any interaction with baseline dietary calcium intake or a dose-response relation suggests that increasing intake through dietary sources or through supplements does not correct a dietary deficiency in which case greater effects would be seen in those with the lowest intakes or the highest doses.

Conclusions In summary, increasing calcium intake from dietary sources increases BMD by a similar amount to increases in BMD from calcium supplements. What this study adds Increasing calcium intake either by dietary sources or supplements has small non-progressive effects on bone density These effects are unlikely to translate into clinically meaningful reductions in fractures. Notes Cite this as: BMJ ;h Ethical approval: Not required. Data sharing: No additional data available. JAMA ; : IOM Institute of Medicine. Dietary reference intakes for calcium and vitamin D.

National Academies Press, Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures and bone loss in people aged 50 years and older: a meta-analysis. Lancet ; : Vascular events in healthy older women receiving calcium supplementation: randomised controlled trial. BMJ ; : Effect of calcium supplements on risk of myocardial infarction and cardiovascular events: meta-analysis. BMJ ; : c BMJ ; : d Calcium plus vitamin D supplementation and the risk of fractures.

N Engl J Med ; : Adverse events from calcium supplementation: relationship to errors in myocardial infarction self-reporting in randomized controlled trials of calcium supplementation. J Bone Miner Res ; 27 : Bauer DC. Clinical practice. Calcium supplements and fracture prevention. Calcium intake and risk of fracture: systematic review. BMJ ; : h Cochrane handbook for systematic reviews of interventions. Version 5. Cochrane Collaboration, Hansson T, Roos B.

The effect of fluoride and calcium on spinal bone mineral content: a controlled, prospective 3 years study. Calcif Tissue Int ; 40 : Effect of calcium or 25OH vitamin D3 dietary supplementation on bone loss at the hip in men and women over the age of J Clin Endocrinol Metab ; 85 : Age Ageing ; 33 : 45 Bone mineral density and bone markers in patients with a recent low-energy fracture: effect of 1 y of treatment with calcium and vitamin D.

Am J Clin Nutr ; 86 : The effect of milk supplements on calcium metabolism, bone metabolism and calcium balance. Am J Clin Nutr ; 41 : Effect of calcium supplementation on forearm bone mineral content in postmenopausal women: a prospective, sequential controlled trial. J Nutr ; : A 1-y walking program and increased dietary calcium in postmenopausal women: effects on bone.

Am J Clin Nutr ; 53 : Effects of calcium supplements on femoral bone mineral density and vertebral fracture rate in vitamin-D-replete elderly patients. Osteoporos Int ; 4 : The effects of calcium supplementation milk powder or tablets and exercise on bone density in postmenopausal women. J Bone Miner Res ; 10 : Calcium supplementation prevents seasonal bone loss and changes in biochemical markers of bone turnover in elderly New England women: a randomized placebo-controlled trial.

J Clin Endocrinol Metab ; 83 : Preventing postmenopausal bone loss with ossein-hydroxyapatite compounds. Results of a two-year, prospective trial. J Reprod Med ; 44 : OpenUrl PubMed. An open, crossover trial of calcium-fortified milk in prevention of early postmenopausal bone loss. Med J Aust ; : Milk supplementation of the diet of postmenopausal Chinese women on a low calcium intake retards bone loss. J Bone Miner Res ; 16 : The effect of milk supplementation on bone mineral density in postmenopausal Chinese women in Malaysia.

Osteoporos Int ; 14 : Comparison of the effects of two different types of calcium supplementation on markers of bone metabolism in a postmenopausal osteopenic population with low calcium intake: a double-blind placebo-controlled trial. Climacteric ; 7 : 33 Calcium- and vitamin D3-fortified milk reduces bone loss at clinically relevant skeletal sites in older men: a 2-year randomized controlled trial. J Bone Miner Res ; 21 : Changes in biochemical indexes of bone metabolism and bone mineral density after a mo dietary intervention program: the Postmenopausal Health Study.

Effects of a multi-component exercise program and calcium-vitamin-D3-fortified milk on bone mineral density in older men: a randomised controlled trial. Osteoporos Int ; 20 : Osteoporos Int ; 23 : Effect of estrogens and calcium carbonate on bone loss in postmenopausal women. Ann Intern Med ; 87 : Acta Orthop Scand ; 49 : Physical activity and calcium modalities for bone mineral increase in aged women. Med Sci Sports Exerc ; 13 : 60 Does calcium supplementation prevent postmenopausal bone loss? A double-blind, controlled clinical study. Calcium supplementation and bone loss in middle-aged women.

Am J Clin Nutr ; 50 : A controlled trial of the effect of calcium supplementation on bone density in postmenopausal women. Increase of bone mineral density by calcium supplement with oyster shell electrolysate. Bone Miner ; 11 : 85 The rate of bone mineral loss in normal men and the effects of calcium and cholecalciferol supplementation. Ann Intern Med ; : 29 Calcium supplementation reduces vertebral bone loss in perimenopausal women: a controlled trial in women between 46 and 55 years of age. J Clin Endocrinol Metab ; 73 : Prevention of postmenopausal osteoporosis.

A comparative study of exercise, calcium supplementation, and hormone-replacement therapy. Vitamin D3 and calcium to prevent hip fractures in the elderly women. The effects of calcium supplementation and exercise on bone density in elderly Chinese women. Osteoporos Int ; 2 : Effect of calcium supplementation on bone loss in postmenopausal women. Calcium supplementation with and without hormone replacement therapy to prevent postmenopausal bone loss.

Calcium deficiency | pathology |

Ann Intern Med ; : 97 Spinal bone loss in postmenopausal women supplemented with calcium and trace minerals. Heated oyster shell-seaweed calcium AAA Ca on osteoporosis. Calcif Tissue Int ; 58 : Maturitas ; 23 : Correcting calcium nutritional deficiency prevents spine fractures in elderly women. J Bone Miner Res ; 11 : Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older.

Calcium and vitamin D supplementation increases spinal BMD in healthy, postmenopausal women. Osteoporos Int ; 8 : Calcium supplementation suppresses bone turnover during weight reduction in postmenopausal women. J Bone Miner Res ; 13 : Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women. The effect of calcium citrate on bone density in the early and mid-postmenopausal period: a randomized placebo-controlled study. Am J Ther ; 6 : J Bone Miner Metab ; 18 : Effect of oral therapy with alphacalcidol or calcium in Korean elderly women with osteopenia and low dietary calcium.

Nutr Res ; 21 : OpenUrl CrossRef. Combined calcium and vitamin D3 supplementation in elderly women: confirmation of reversal of secondary hyperparathyroidism and hip fracture risk: the Decalyos II study. Osteoporos Int ; 13 : Effects on bone mineral density of calcium and vitamin D supplementation in elderly women with vitamin D deficiency. Joint Bone Spine ; 70 : The effect of calcium and vitamin D3 supplementation on the healing of the proximal humerus fracture: a randomized placebo-controlled study.

Calcif Tissue Int ; 75 : Supplementation with oral vitamin D3 and calcium during winter prevents seasonal bone loss: a randomized controlled open-label prospective trial. J Bone Miner Res ; 19 : J Bone Miner Res ; 20 : Effects of calcium supplementation on clinical fracture and bone structure: results of a 5-year, double-blind, placebo-controlled trial in elderly women.

Arch Intern Med ; : Randomized controlled trial of calcium in healthy older women. Am J Med ; : Two-year randomized controlled trial of vitamin K1 phylloquinone and vitamin D3 plus calcium on the bone health of older women. J Bone Miner Res ; 22 : Treatment with alendronate plus calcium, alendronate alone, or calcium alone for postmenopausal low bone mineral density. Curr Med Res Opin ; 23 : Randomized controlled trial of calcium supplementation in healthy, nonosteoporotic, older men.

Effects of calcium and vitamin D supplementation on hip bone mineral density and calcium-related analytes in elderly ambulatory Australian women: a five-year randomized controlled trial. J Clin Endocrinol Metab ; 93 : Discrepant influence of vitamin D status on parathyroid hormone and bone mass after two years of calcium supplementation. Clin Endocrinol Oxf ; 73 : The efficacy of calcium supplementation alone in elderly Thai women over a 2-year period: a randomized controlled trial. Osteoporos Int ; 24 : Does daily vitamin D IU and calcium mg supplementation decrease the risk of falling in ambulatory women aged years?

Maturitas ; 65 : Effect of low-dose calcium supplements on bone loss in perimenopausal and postmenopausal Asian women: a randomized controlled trial. Later in the life cycle, women continue to be at highest risk and this risk is elevated if early baseline bone is not strong during adolescence. Women who have diagnosed eating disorders or exhibit physical hyperactivity with female athlete triad syndrome have been shown to be at high risk for calcium deficiency. Postmenopausal women, due to hormonal changes that may affect bone mineralization processes, have also been widely studied for calcium deficiency risk [ 3 , 5 ].

Individuals with milk allergy or lactose intolerance often exhibit calcium deficiency due to the dietary restriction of calcium-containing foods. These individuals can be effectively treated with dietary modifications which will be discussed later in the manuscript [ 6 ]. Both adolescents and elderly populations often have high risk of calcium deficiency due to dietary habits. Adolescents throughout the world are growing in risk due to dietary pattern changes. Many adolescents decrease calcium intake by substituting dairy products particularly beverages or by decreasing total intake of calcium.

Eating disorders in both male and female teens may result in nutrient deficiencies that include calcium. The elderly are at risk for multiple reasons including low calcium intake over time, medication interactions that may decrease dietary calcium absorption, and the underlying chronic disease osteoporosis which changes bone formation and strength [ 1 , 3 , 7 , 8 ].

Table 1 lists dietary recommendations for key nutrients in selected populations including healthy adults and at-risk populations. The minimum requirement is mg per day for calcium. Dietary recommendations are established to prevent nutrient deficiencies [ 1 , 3 , 8 , 9 , 10 , 11 , 12 ]. Nutrient recommendations for healthy adults for calcium, phosphorus, vitamin D, and protein by country. However, many individuals both young and old are deficient. In the United States as in many countries, there are deficiencies in population groups. In the United States, current predominant sources of calcium in the diet include dairy products milk, yogurt, cheese and commercially fortified foods orange juice, cereals, breads [ 1 , 3 ].

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The most predominant food sources include dairy but also anchovy, soy, and kimchi [ 9 , 10 , 11 , 12 ]. A wide variety of foods is necessary to achieve dietary guidelines.

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This reinforces that eating one single food or food group will not achieve dietary balance. It is important to remember that it is difficult if not impossible to discuss calcium alone. Calcium metabolism is a collaborative effort between calcium, phosphorus, vitamin D, and protein.

Just like a musical orchestra, all of these nutrients are needed to create the end product whether it is a beautiful song or a perfect bone matrix. Calcium comprises a complex interactive dependency on the actions of other nutrients. Dietary calcium must move across the intestinal lumen during normal digestion to provide a calcium pool to maintain serum levels. However, dietary protein is required to provide serum IGF-1 which in turns interacts with the renal system to transform vitamin D to an active form. The resulting vitamin D receptor transcription provides the necessary substrates to move the calcium across luminal, basolateral, or intercellular compartments as needed to maintain serum levels.

Without these interval steps, calcium would not be available to replace and maintain serum pools. Each step requires an interaction with another nutrient [ 16 , 17 ]. A recent meta-analysis by Fenton and colleagues illustrated the dependent relationship between phosphate and changes in calcium balance that occur primarily in the kidney.

This research showed an inverse correlation between decreases in urinary calcium with increasing phosphate doses while demonstrating that calcium balance increases proportionately with phosphate. Particularly during periods of growth, foods that contain both calcium and phosphorus can lead to positive effects on bone health [ 18 ]. Cumulative research by Heaney and colleagues help understand the strong correlation between vitamin D level and calcium absorption. The work has reinforced the concept that teams of nutrients collaborate to control and maintain serum levels within the human body.

This compensatory mechanism shows the unique communication system which directly affects how much of an available nutrient is absorbed and the signaling mechanism to change metabolic pathways to adjust transport. These mechanisms help changes in dietary intake and available nutrients to undergo adaptation at the system level to assure consistent nutrients for metabolic functions [ 16 , 19 ]. There are tissue-specific effects of inadequate calcium and vitamin D on both plasma serum calcium and vitamin D. The role of calcium-sensing receptors that direct metabolic changes to maintain normal extracellular calcium levels is only beginning to be understood.

Calcium-sensing receptor cells are found primarily on the parathyroid glands but are also located in other areas of the body.

They have been shown through research to detect even the smallest changes in serum calcium and look for immediate sources of cellular calcium to restore plasma levels to the normal range. Low plasma vitamin D will also decrease enzymatic OHD-one-alpha-hydroxylase activity. This in turn may change the normal differentiation and proliferation of bone and intestinal cells. Deficiencies in both dietary calcium and vitamin D will impair the function of these mechanisms and others to restore serum calcium. Long term deficiencies set the stage for chronic disease risk [ 2 , 15 , 17 , 20 ].

Saropenia is a term used to describe loss of muscle strength and mass. It is a leading cause of fall risk. Adequate dietary protein is needed to provide the amino acids required for muscle protein synthesis. The quality of the protein is also important. Dairy products are good sources of these nutrients because they contain the amino acid leucine as well as calcium to support both muscle and bone maintenance. Fall risk can be reduced by consuming adequate protein that also contains calcium [ 21 , 22 , 23 , 24 ].

A very simplified explanation of bone formation will be used to help understand the true complexity of this ongoing lifecycle process.

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To create new bone or maintain bone composition, bone-forming cells osteoblasts migrate into the non-mineralized matrix vesicles structure. This is followed by attraction of phosphorus and then calcium ions to create the mineralization density of the bone. On the cellular level, sodium phosphorus transporter protein molecules create the hydroxyapatite crystals as the precursor of the actual bone mineralization. Both phosphorus and calcium play essential interdependent roles in the formation of both new bone and repair of existing bone [ 15 , 17 , 25 ].

The priorities of bone formation differ by population group. In children and young adults, emphasis is placed on strong baseline bone growth and structure as a foundation. By ages , the majority of new bone formation is completed. After this growth period, emphasis is placed on maintaining bone density and preventing loss. After the age of 50, research has shown bone density often decreases substantially so the goal at this life cycle phase is to sustain bone mineral density and minimize bone loss.

Progressive bone mineralization loss over time increases the risk of bone fracture and falling [ 1 , 23 , 26 ]. In the United States, more than 1. Several recent meta-analyses have correlated a higher calcium dietary intake to reduced fracture risk. A meta-analysis by Boonen and colleagues compared randomized clinical trials in the published literature between vitamin D alone versus vitamin D and calcium. All trials had a placebo group. Results confirmed the use of vitamin D with calcium resulted in a statistically significant reduction in hip fracture compared to the placebo group [ 21 ].

Reid and colleagues updated a prior meta-analysis to include randomized controlled studies from more than 30, total patients. Adequate nutrition is an underlying principle to bone maintenance. All calories are not the same. Foods must be chosen wisely to provide nutrient density of key nutrients of calcium, phosphorus, vitamin D, and protein. The required dietary intake of all four of these nutrients is necessary to support the overall goal of reducing fracture risk through partnerships with bone formation, bone mineralization, muscle mass and strength.

Chronic deficiency of these interactive nutrients will result in an increased in fall risk particularly in the elderly. It is logical that adequate nutrition in adolescent and adults years helps create stronger bones with age [ 1 , 11 , 24 ]. A study of adults over the age of 50 found the highest risk in those consuming less than 1, mg of dietary calcium per day assessed by food frequency questionnaire.

This study infers that it is important to evaluate the nutrition status of all adults since many of these individuals had normal bone mineral density using standardized methodology. This study also supported an individualized calcium intake based on fracture risk [ 28 ]. The population group at lowest risk for osteoporosis consumed a high quality diet that included adequate amounts of fruits, vegetables, and calcium.

These individuals also had a higher serum vitamin D which is consistent with the findings linking low serum vitamin D with higher fracture risk. Moderate physical activity in conjunction with healthy body weight may contribute to the muscle mass and strength as well as bone density reducing osteoporosis risk. This evidence-based consensus report recommended adequate dietary calcium as an effective treatment option in both men and women who already had bone density and osteoporosis.

The education message is that dietary adequacy through food or supplementation may help sustain or improve bone composition even when overt bone changes are already present [ 26 ].

The research literature continues to discuss multiple viewpoints on the relationship between calcium and cardiovascular disease. A major controversy lies in understanding where the calcium deposits in the soft tissue originated and what metabolic process is responsible for their formation. Many of the published analyses are retrospective using large databases which may have poor long term dietary information.

It is important also to argue that the investigation of single nutrients rather than complex dietary patterns is difficult to assess. Many confounding variables are present such as physical activity and genetic predisposition that are difficult to control for in the statistical methods. The risk information is evolving and professionals need to keep updated on the emerging data [ 29 , 30 , 31 ].

A recent published analysis compared five similar trials of calcium supplementation including the Womens' Health Initiative cohort. All of these trials used calcium supplementation rather than increase in dietary intake to achieve intervention levels. The higher risk with calcium supplementation alone compared to dietary intervention alone appears to support adequate intake by food as a more effective strategy [ 27 ].

Several reviews and individual studies have provided support that consuming a diet adequate in calcium may help in maintaining normal body weight and decreasing the risk of obesity. This is consistent with both Korean and global recommendations to include dietary sources of calcium to decrease chronic disease risk and promote preventive health [ 15 , 20 , 32 , 33 , 34 ]. In another recent systematic review and meta-analysis, 14 studies were analyzed to quantify the amount of dairy product consumption that was linked to lower incidence of type 2 diabetes.

Other studies have documented the role of calcium through dairy products consumption with diabetes risk reduction [ 36 ]. Ideally, a varied and diverse diet should be able to provide adequate intake of the calcium and key supportive nutrients. Diet and food are the preferred methods to achieve dietary goals. However, oral calcium supplementation may be required. Different calcium compounds may have different absorption rates. Most are absorbed in the ileum where the pH level promotes degradation and transport.

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The use of vitamin D in conjunction with oral calcium supplements is more effective than calcium alone [ 1 , 27 ]. Lactase is the enzyme specific to the breakdown of the sugar lactose found primarily in dairy products. The majority of individuals who are milk intolerant have lactase deficiency, not milk allergy. Milk allergy would require a diagnosis of an immunological response to milk protein.

Lactase production decreases naturally with age and also declines when an individual stops consuming lactose in their diet. Asian populations as well as African Americans are often lactase deficient. Also, as people age lactase deficiency appears to be more common [ 1 , 6 ]. Most individuals manufacture some lactase but may be unable to produce sufficient quantities to handle a load of mL of milk at one meal.

Consuming lactose-containing foods in conjunction with a meal appear to decrease symptoms in many individuals. Therefore, it is recommended to gradually introduce small amounts of lactose-containing foods. This strategy may help to stimulate the gastrointestinal tract to increase production of lactase or determine the maximum quantity that can be consumed at a single meal or snack [ 6 ]. Another strategy is to start by introducing dairy foods with a higher fat content to delay gastrointestinal transit and potentially allow for a longer time for the lactase to be available during the digestion process.

Higher fat dairy often contain amounts of calcium so habitual intake will not address dietary adequacy. However, this strategy may lower the fear of trying new dairy foods if they can successfully consume ice cream or add cream to their cereal. Different foods have different lactose content.

Tables of lactose content of foods can be found from government sources [ 1 ]. Fermented foods such as kimchi and aged cheeses are lower in lactose content. Lowering the lactose content does not lower the calcium content. Other strategies to address lactose intolerance or lactase deficiency include specialty products. Lactose-free or lactosereduced commercial products are available in the United States, Korea, and other countries. Lactase tablets or drops can also be added to foods themselves [ 6 ].

In the United States, there are an increasing number of new dairy products for consumers to try than emphasize more natural taste and formulas. Greek-style yogurt has become very popular primarily because its consistency is thicker.

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There is also a new soft cheese in the French "creme fraiche" style that is sold in smaller four-ounce portions which is thicker, more tart, and less sweet. The trend in the United States is moving away from thinner, sweeter yogurt products that were thickened with gelatin and often tasted artificial. It provides a considerable amount of positive bio-bacteria to keep the gastrointestinal flora healthy. Consumption of keifer and other active fermented dairy products on a regular basis can help establish and maintain a healthy gut flora.

This is particularly important after a course of oral antibiotics which may have reduced, changed, or destroyed gut microbial diversity. In summary, this narrative review has emphasized the following key information regarding calcium through the lifecycle. Calcium consumed as food naturally contains many other nutrients and should be primary method of intake. Calcium supplements may be required to correct deficiencies particularly in at risk populations. Barriers to adequate intake need to be addressed including lactase deficiency and innovative ways to increase intake with at risk populations.

No conflict interests were declared by the author. National Center for Biotechnology Information , U. Journal List Clin Nutr Res v. Clin Nutr Res. Published online Jan Judith A.

Adequacy of calcium intake during pregnancy in a tertiary care center

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