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Calcium supplementation during pregnancy and lactation: Effects on the mother and the fetus

      Calcium consumption is essential for bone development and maintenance throughout life, yet more than one half of the female population in the United States does not consume the recommended amount of calcium. Calcium intake is especially crucial during pregnancy and lactation because of the potential adverse effect on maternal bone health if maternal calcium stores are depleted. There is often a transient lowered bone mineral density and increased rate of bone resorption, with the greatest consequence during the third trimester and throughout lactation. Studies indicate that calcium consumption should be encouraged, especially during pregnancy and lactation, to replace maternal skeletal calcium stores that are depleted during these periods. Because the fetus in utero and the neonate through breast-feeding are dependent on maternal sources for the total calcium load, adequate maternal calcium intake also can affect fetal bone health positively. Proper calcium consumption can be attained through the diet by the consumption of dairy products or leafy greens (such as kale), the consumption of fortified foods, or by supplementation with widely available calcium-containing supplement products. Because many women experience heartburn during pregnancy, calcium-based antacids are ideal for providing heartburn relief, and they offer a calcium supplement to ensure maternal and fetal bone health, without the danger of adverse effects on the neonate.

      Key words

      Calcium is a critical component of human bone and contributes 1% to 2% of body mass.
      • Institute of Medicine
      DRI dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride.
      Calcium is necessary for numerous physiologic functions. Because calcium cannot be manufactured within the body, all needed calcium must be consumed dietarily through the gastrointestinal tract, after which it is transferred to the skeletal system, where 98% of the calcium is stored.
      • Prentice A.
      Calcium in pregnancy and lactation.
      In addition to contributing to skeletal strength, calcium stores are concentrated in teeth and bone serve as reservoirs for a variety of physiologic functions during periods of decreased calcium consumption or increased calcium mobilization. As such, when insufficient calcium is consumed to meet these needs, depletion of calcium stores in the bone can weaken the skeletal system.
      • Heaney R.P.
      Calcium, dairy products and osteoporosis.
      Bone is in a dynamic constructive and destructive balance. This is relevant to both the young and old when this equilibrium is compromised by the stress of gaining or losing bone mass. Increased calcium intake is well-recognized as necessary in perimenopausal women to reduce skeletal weakening and is associated with a decreased fracture risk, which is a consequence of osteopenia and osteoporosis.
      • Tresolini C.P.
      • Gold D.T.
      • Lee L.S.
      Working with patients to prevent, treat, and manage osteoporosis: a curriculum guide for the health professions.

      US Department of Health and Human Services. Report of the Surgeon General's workshop on osteoporosis and bone health (web page); posted December 2002; last accessed June 28, 2004. Available at: http://www.surgeongeneral.gov/library/bonehealth/content.html.

      An inverse correlation also exists between calcium consumption and other ailments, which include colon cancer,
      • Wallace K.
      • Baron J.A.
      • Cole B.F.
      • Sandler R.S.
      • Karagas M.R.
      • Beach M.A.
      • et al.
      Effect of calcium supplementation on the risk of large bowel polyps.
      thereby making calcium intake important beyond bone health at all stages of life.
      The benefits of calcium are well-recognized by the general public. However, turning this high awareness into action has proved difficult, which is exemplified by the fact that less than one half of the female population meets the recommended intake. In fact, studies show that only 16% of women consume the minimum 2 recommended servings of dairy each day (Table I).
      • US Department of Health and Human Services, Health Resources and Services Administration Maternal and Child Health Bureau
      Women's health USA 2003.
      Ironically, 63.5% of adults who believe that they consume the correct amount of calcium actually consume less than the recommended daily levels,

      US Department of Agriculture, Agricultural Research Service. Results from USDA's 1994-1996 diet and health knowledge survey: table set 19 (web page); posted October 2000; last accessed July 8, 2004. Available at: http://www.barc.usda.gov/bhnrc/foodsurvey/home.htm.

      which suggests that education regarding an individual's calcium “state” would be beneficial. Furthermore, at no stage in a woman's life are the recommended intake levels for calcium achieved.
      • Ervin R.B.
      • Wang C.Y.
      • Wright J.D.
      • Kennedy-Stephenson J.
      Dietary intake of selected minerals for the United States population: 1999-2000: advance data from vital and health statistics; no. 341.
      As a result, there are important implications during particular life stages (eg, pregnancy, lactation, and menopause).
      Table IDietary calcium sources
      Food sourceServing size (oz)Calcium content per serving (mg)
      Low-fat plain yogurt8415
      Low-fat yogurt with fruit8245-384
      Sardines3324
      Cheddar cheese, shredded1.5306
      Skim milk8302
      2% Low-fat milk8297
      Whole milk8291
      Buttermilk8285
      Mozzarella, part skim1.5275
      Tofu, firm4205
      Orange juice, calcium fortified6200-260
      Salmon with bones3181
      Pudding, chocolate w/2% milk4153
      Cottage cheese 1% milk fat8138
      Tofu, soft4138
      Spinach, cooked4120
      Frozen yogurt, vanilla, soft serve4103
      Turnip greens, boiled499
      Kale, cooked894
      Kale, raw890
      Ice cream, vanilla485
      Bread, white131
      Broccoli, raw421
      Adapted from the Office of Dietary Supplements, 2004. Available at: http://ods.od.nih.gov/factsheets/calcium.asp.
      Important points at which calcium intake is critical are pregnancy and nursing. During pregnancy, the growing fetus receives its total nourishment from maternal sources.
      • Institute of Medicine
      DRI dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride.
      The dynamic balance between skeletal calcium storage and fetal nutritional needs can affect the maternal calcium equilibrium adversely. Therefore, if adequate bone has not been built before pregnancy and adequate calcium is not part of the maternal diet, bone can be degraded as calcium is taken from the maternal skeleton.
      This maternal calcium deficit during pregnancy and lactation greatly depletes maternal calcium stores as the fetus accumulates 25 to 30 g of calcium over the course of pregnancy.

      Drinkwater BL, Chesnut CH 3rd. Bone density changes during pregnancy and lactation in active women: a longitudinal study. Bone Miner 1991;14:153-60.

      The greatest maternal-fetal calcium transfer occurs during the third trimester.
      • Givens M.H.
      • Macy I.G.
      The chemical composition of the human fetus.
      At 20 weeks of gestation, the fetal calcium accretion rate is 50 mg/d and increases to 330 mg/d at 35 weeks.
      • Prentice A.
      Calcium in pregnancy and lactation.
      During the postpartum period, a large amount of calcium is transferred to the neonate through nursing, which accounts for approximately 210 mg/d.
      • Institute of Medicine
      DRI dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride.
      Fetal calcium needs are met through the extraction of calcium from maternal bone mass, increased intestinal absorption, or decreased renal excretion.
      • Prentice A.
      • Jarjou L.M.
      • Cole T.J.
      • Stirling D.M.
      • Dibba B.
      • Fairweather-Tait S.
      Calcium requirements of lactating Gambian mothers: effects of a calcium supplement on breast-milk calcium concentration, maternal bone mineral content, and urinary calcium excretion.
      To meet this increased skeletal stress, the Institute of Medicine currently recommends 1000 mg/d of calcium for pregnant and lactating women who are 19 to 50 years old and 1300 mg/d for pregnant and lactating women who are <19 years old.
      • Institute of Medicine
      DRI dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride.
      The failure to meet this guideline is highlighted by the fact that only 6% of childbearing women report consuming the recommended daily amount of calcium,

      March of Dimes Birth Defect Foundation. During your pregnancy: do you get enough calcium every day? (web page). Accessed July 8, 2004. Available at: http://www.marchofdimes.com.

      with actual daily intakes near 50% to 70% of the recommended intake (Table II).
      • Chang S.C.
      • O'Brien K.O.
      • Nathanson M.S.
      • Caulfield L.E.
      • Mancini J.
      • Witter F.R.
      Fetal femur length is influenced by maternal dairy intake in pregnant African American adolescents.
      • Harville E.W.
      • Schramm M.
      • Watt-Morse M.
      • Chantala K.
      • Anderson J.J.
      • Hertz-Picciotto I.
      Calcium intake during pregnancy among white and African-American pregnant women in the United States.
      • US Department of Agriculture, Center for Nutrition Policy and Promotion. Federal Studies
      Review of the nutritional status of WIC participants.
      Table IICalcium Recommendations for Women
      Age (years)Adequate Daily intakes (mg/day)Mean Daily intake (mg/day)
      14-181300793
      19-391000797
      Adapted from the DRI reports at the USDA Food and Nutrition Information Center, 2004 and Ervin, 2004.
      According to the Women Physicians' Health Study, 47% of the 87 pregnant female physicians consumed calcium-containing supplements, compared with only 29% of 1148 nonpregnant 30- to 40-year-old physicians who were surveyed. Also, 36% of the 30- to 40-year-old pregnant physicians averaged >1 calcium supplement each day; only 15% of the 30- to 40-year-old nonpregnant physicians used them with the same frequency.
      • Frank E.
      • Cone K.
      Characteristics of pregnant vs. non-pregnant women physicians: findings from the women physicians' health study.
      Physicians' personal health practices are of particular interest because they affect their patient care. A direct relationship exists between physicians' personal health behaviors and their ability to motivate patients.
      • Frank E.
      • Breyan J.
      • Elon L.
      Physician disclosure of healthy personal behaviors improves credibility and ability to motivate.
      Also, physicians who practice a certain behavior, such as calcium supplementation use, are more likely to speak to their patients about the behavior, which increases compliance and awareness.
      • Frank E.
      • Rothenberg R.
      • Lewis C.
      • Belodoff B.F.
      Correlates of physicians' prevention-related practices: findings from the Women Physicians' Health study.
      Dietary calcium is found primarily in dairy foods. Although milk is the most commonly consumed dairy product, the national consumption of milk has decreased drastically over the last century,
      • Putnam J.J.
      • Allshouse J.E.
      Food consumption, prices, and expenditures, 1970-97: statistical bulletin no. 965.
      with detrimental consequences for the nation's overall calcium levels. Based on the deficit in calcium intake from food sources, other options for ensuring adequate intake are necessary. Calcium supplements are a viable source of calcium that can be used to augment often insufficient dietary calcium intakes. Potential calcium sources, often unrecognized by women, include calcium-containing antacids, which are used routinely by women to treat heartburn symptoms that are associated with pregnancy.
      Calcium-based antacids come in a variety of forms that use different salts; the 2 most common salts are calcium carbonate and calcium citrate. Comparative studies of the absorbability of these 2 salts have shown calcium carbonate and calcium citrate to be equally well absorbed when taken with food, with further investigation demonstrating that calcium carbonate and calcium citrate provide bioavailable calcium equally as well as dietary sources such as milk and calcium-fortified orange juice. Although, because calcium carbonate supplements have the highest percentage of elemental calcium among the calcium salts, they are generally considered the most cost-effective form and should be the first choice for most patients. In addition, because calcium carbonate has approximately twice as much elemental calcium as calcium citrate, it requires fewer tablets to achieve a given dose of elemental calcium, which results in a decreased cost for the patient and a potentially increased rate of patient compliance.
      Previous review articles have been published regarding maternal calcium requirements during pregnancy and lactation and have concluded that the lack of available evidence restricts the ability to form strong conclusions, especially with respect to supplementation's effect on maternal bone health during pregnancy.
      • Prentice A.
      Calcium in pregnancy and lactation.
      • Kalkwarf H.J.
      • Specker B.L.
      Bone mineral changes during pregnancy and lactation.
      • Prentice A.
      Maternal calcium metabolism and bone mineral status.
      Yet, more recently published studies urge a re-evaluation of the evidence.
      • Chang S.C.
      • O'Brien K.O.
      • Nathanson M.S.
      • Caulfield L.E.
      • Mancini J.
      • Witter F.R.
      Fetal femur length is influenced by maternal dairy intake in pregnant African American adolescents.
      • Janakiraman V.
      • Ettinger A.
      • Mercado-Garcia A.
      • Hu H.
      • Hernandez-Avila M.
      Calcium supplements and bone resorption in pregnancy: a randomized crossover trial.
      In this re-evaluation, data are presented to support the theory that, to protect against loss of bone mass, calcium intake should be supplemented through diet or other means to attain or exceed the recommended intake values during the reproductive period. In addition to ensuring optimal maternal bone health, increased calcium intake should increase the amount of calcium that is available to the fetus during pregnancy and the infant while breast-feeding.

      Evidence for bone loss during pregnancy and lactation

      Numerous studies have demonstrated significant decreases in bone mineral indicators in pregnant and lactating women, with the greatest change occurring during the third trimester and lactation. These are the periods when the greatest maternal-fetal calcium transfer takes place.

      Drinkwater BL, Chesnut CH 3rd. Bone density changes during pregnancy and lactation in active women: a longitudinal study. Bone Miner 1991;14:153-60.

      • Affinito P.
      • Tommaselli G.A.
      • di Carlo C.
      • Guida F.
      • Nappi C.
      Changes in bone mineral density and calcium metabolism in breastfeeding women: a one year follow-up study.
      • Kent G.N.
      • Price R.I.
      • Gutteridge D.H.
      • Allen J.R.
      • Rosman K.J.
      • Smith M.
      Effect of pregnancy and lactation on maternal bone mass and calcium metabolism.
      Measurements of bone health are provided as bone mineral density (BMD) value, which is a measurement of the density of the bone in grams per cubic centimeter, or bone mineral content (BMC), which is a measurement of the mass of the bone in grams. Reductions in total BMD values up to 3.6% have been detected.
      • Sowers M.F.
      • Scholl T.
      • Harris L.
      • Jannausch M.
      Bone loss in adolescent and adult pregnant women.
      Decreases at the lumbar region have been observed, as well as at the hip, femoral neck, ultradistal radius, and trochanter. In a study by Pearson et al,
      • Pearson D.
      • Kaur M.
      • San P.
      • Lawson N.
      • Baker P.
      • Hosking D.
      Recovery of pregnancy mediated bone loss during lactation.
      >5% of bone mass can be lost at the spine, sometimes reaching 7%. Another study demonstrated that markers of bone turnover are increased greatly during pregnancy, which indicates an increase in bone resorption and a decline in bone health.
      • Naylor K.E.
      • Iqbal P.
      • Fledelius C.
      • Fraser R.B.
      • Eastell R.
      The effect of pregnancy on bone density and bone turnover.
      Although some of the bone mass that is lost during lactation is regained after weaning, the bone mass only partially returns to prepregnancy values. The rate of bone loss during pregnancy and lactation is greater than the annual rate of loss in women after menopause.
      • Kalkwarf H.J.
      • Specker B.L.
      Bone mineral changes during pregnancy and lactation.
      Therefore, adequate calcium consumption is vital, especially for pregnant and lactating women.

      Impact of increased calcium intake

      Studies have indicated that an increased calcium intake reduces, and in some cases counteracts, the reduction of maternal bone during pregnancy and lactation. We will summarize a number of studies that examine maternal and fetal bone health as a function of calcium intake, either through dietary means or a calcium supplement, through pregnancy, lactation, and weaning.
      Based on the fact that physiologic demands are different for each of these stages, each stage has been evaluated separately. In lactation and weaning studies, we evaluate studies of the effects of an increased intake of dietary calcium, a study that incorporated both dietary and supplemental calcium, and studies that involved only calcium supplements. The evidence indicates that the beneficial effects of calcium can be obtained equally from both diet and supplementation.

      Pregnancy

      A wealth of information exists to indicate that increased calcium intake and calcium supplementation improves bone health throughout the lifespan.
      • Aloia J.F.
      • Vaswani A.
      • Yeh J.K.
      • Ross P.L.
      • Flaster E.
      • Dilmanian F.A.
      Calcium supplementation with and without hormone replacement therapy to prevent postmenopausal bone loss.
      • Fujita T.
      • Ohue T.
      • Fujii Y.
      • Miyauchi A.
      • Takagi Y.
      Effect of calcium supplementation on bone density and parathyroid function in elderly subjects.
      • Ginty F.
      • Flynn A.
      • Cashman K.D.
      The effect of short-term calcium supplementation on biochemical markers of bone metabolism in healthy young adults.
      Yet, there are limited studies regarding the effect of supplementation during pregnancy because of medical/legal/ethical concerns (Table III). Janakiraman et al
      • Janakiraman V.
      • Ettinger A.
      • Mercado-Garcia A.
      • Hu H.
      • Hernandez-Avila M.
      Calcium supplements and bone resorption in pregnancy: a randomized crossover trial.
      published 1 of the first papers to examine the effect of calcium supplementation during pregnancy on the rates of maternal bone resorption.
      Table IIIMaternal studies
      StudyPopulationCalcium source/dosageOutcomes
      Janakiraman, 2003
      • Janakiraman V.
      • Ettinger A.
      • Mercado-Garcia A.
      • Hu H.
      • Hernandez-Avila M.
      Calcium supplements and bone resorption in pregnancy: a randomized crossover trial.
      31 pregnant Mexican women, 25 to 35 weeks gestation1200 mg/day supplement14% decrease NTX
      Cross, 1995
      • Cross N.A.
      • Hillman L.S.
      • Allen S.H.
      • Krause G.F.
      Changes in bone mineral density and markers of bone remodeling during lactation and postweaning in women consuming high amounts of calcium.
      Baseline to lactation15 lactating women, 2 weeks postpartum to 3 months lactation1 g/day calcium carbonate supplement5.7% BMD gain at ultradistal site in calcium group
      Lactation to postweaning15 lactating women, 3 months lactation to 3 months post-weaning1 g/day calcium carbonate supplement3% BMD gain at lumbar region in calcium group, no statistical gain in placebo group
      5.2% BMD loss at ultradistal site in placebo, no statistical loss in calcium group
      Kalkwarf, 1997
      • Kalkwarf HJ.
      • Specker B.L.
      • Bianchi D.C.
      • Ranz J.
      • Ho M.
      The effect of calcium supplementation of bone density during lactation after weaning.
      Lactation study97 lactating women, 99 non-lactating women, 2 weeks to 6 months postpartum1 g/day calcium carbonate supplementSignificant positive effect of calcium supplementation on the lumbar spine region BMD
      Weaning study95 lactating women, 92 non-lactating women, 6 to 12 months postpartum1 g/day calcium carbonate supplementLumbar spine BMD increased significantly more in the calcium group than the placebo group
      Chan, 1987
      • Chan G.M.
      • McMurry M.
      • Westover K.
      • Engelbert-Fenton K.
      • Thomas M.R.
      Effects of increased dietary calcium intake upon the calcium and bone mineral status of lactating adolescent and adult women.
      21 experimental pregnant adolescents, 15 control pregnant adolescents, 12 adults, 1 month pre-partum to 16 weeks postpartumDietary calcium - Experimental: >1600 mg/day Control: 900 mg/day Adult: 1500 mg/dayControl adolescent group decreased BMC 10%, no statistical decrease in high-calcium group
      Krebs, 1997
      • Krebs N.F.
      • Reidinger C.J.
      • Robertson A.D.
      • Brenner M.
      Bone mineral density changes during lactation: maternal, dietary, and biochemical correlates.
      26 lactating women, 8 non-lactating women, 0.5 months to 7 months postpartumDietary calciumHigh calcium intake positively associated with lumbar BMD
      This study evaluated the effect of a 1200 mg/d calcium supplement in 31 pregnant Mexican women in their third trimester (25-35 weeks of gestation) for the effect on the bone resorption marker of cross-linked N-telopeptides of type I collagen.
      • Janakiraman V.
      • Ettinger A.
      • Mercado-Garcia A.
      • Hu H.
      • Hernandez-Avila M.
      Calcium supplements and bone resorption in pregnancy: a randomized crossover trial.
      In this crossover study, subjects in 1 experimental group ingested the calcium supplement for 10 consecutive days and then a multivitamin without calcium for another 10 consecutive days. Nearly 90% of the women showed an average reduction of 14% in N-telopeptides of type I collagen level during the period of calcium supplementation, which indicates that there is a lower rate of bone resorption during the last trimester of pregnancy in those women who receive a calcium-containing supplement than those women without supplementation.

      Lactation

      One study examined BMD values as a function of dietary calcium intake, which demonstrated evidence for the benefits of calcium during lactation.
      • Krebs N.F.
      • Reidinger C.J.
      • Robertson A.D.
      • Brenner M.
      Bone mineral density changes during lactation: maternal, dietary, and biochemical correlates.
      Twenty-six lactating women and 8 nonlactating women were observed for the effect of dietary calcium intake on maternal BMD values from delivery until 7 months after delivery. In the lactating women, dietary calcium intake ranged from 1335 to 1500 mg/d, which is far above the recommended intake values. Based on regression analyses, calcium intake was the only variable among all tested nutrients that was found to be associated positively with BMD values. Throughout the study, calcium intake was associated significantly with increased lumbar spine BMD values.
      In a study of lactating adolescent women, calcium intake and BMC showed a significant positive correlation.
      • Chan G.M.
      • McMurry M.
      • Westover K.
      • Engelbert-Fenton K.
      • Thomas M.R.
      Effects of increased dietary calcium intake upon the calcium and bone mineral status of lactating adolescent and adult women.
      From the last month of pregnancy through 16 weeks after delivery, 21 adolescents consumed a high calcium diet of >1600 mg/d; their results were compared with results for adolescents who consumed their regular diet of 900 mg/d of calcium and adults who consumed 1500 mg/d of calcium. Some individuals in the study used calcium supplements to achieve the target calcium intake of 1600 mg/d. By the end of the trial, the adolescent control group showed a 10% loss in BMC, although the high-calcium diet group showed no decrease in BMC. Bone demineralization occurred only in the adolescent control group. No difference was perceived between those women who relied on dietary calcium only and those women who augmented their diet with a calcium supplement, which suggests that calcium supplementation is a reasonable alternative to the achievement of an adequate dietary calcium intake.
      A randomized trial evaluated the effects of a 1000-mg calcium carbonate supplement on maternal BMD values in lactating women (within 2 weeks after delivery and at 3 months of lactation) and demonstrated less loss of bone mass in the calcium supplement group.
      • Cross N.A.
      • Hillman L.S.
      • Allen S.H.
      • Krause G.F.
      Changes in bone mineral density and markers of bone remodeling during lactation and postweaning in women consuming high amounts of calcium.
      During lactation, a 5.7% gain at the ultradistal radius was observed for the calcium group. This study also included an examination of the weaning/post-weaning period.
      The effect of a 1000-mg/d calcium carbonate supplement on postpartum women who consumed ≤800 mg of dietary calcium daily was evaluated in 2 studies; 1 study examined the effect of the supplement on lactating women.
      • Kalkwarf H.J.
      • Specker B.L.
      • Ho M.
      Effects of calcium supplementation on calcium homeostasis and bone turnover in lactating women.
      In the lactation study, calcium supplementation had an overall significant positive effect on lumbar BMD values. The lactating women who received the calcium supplement only lost 2.4% of their total-body bone mass; the women who received the placebo lost 3.4% of their total-body bone mass.

      Postweaning phase

      In the postweaning phase, Cross et al
      • Cross N.A.
      • Hillman L.S.
      • Allen S.H.
      • Krause G.F.
      Changes in bone mineral density and markers of bone remodeling during lactation and postweaning in women consuming high amounts of calcium.
      demonstrated the beneficial effects of calcium carbonate supplementation. The calcium group significantly increased BMD values at the lumbar region 3%; the placebo group's increase did not reach statistical significance. Significant mean losses of 5.2% were seen at the ultradistal radius in the placebo group. For the entire trial period (baseline through postweaning), the only statistically significant loss was at the ultradistal site in the placebo group, not in the calcium group.
      In the weaning component of the study by Kalkwarf et al,
      • Kalkwarf H.J.
      • Specker B.L.
      • Ho M.
      Effects of calcium supplementation on calcium homeostasis and bone turnover in lactating women.
      significant increases in lumbar BMD values were observed, independent of calcium carbonate supplementation. This supports the theory that bone mass is lost during lactation but is regained after weaning occurs. However, the group that received the calcium supplement increased lumbar bone density significantly more than the placebo group. Although bone mass is regained after weaning occurs whether or not a calcium supplement is ingested, the increase in bone density is much greater with the use of a calcium supplement.

      Fetal bone health

      Studies have been undertaken to examine maternal calcium intake, especially increased intake through supplementation, and its effect on fetal skeletal development, with particular attention paid to fetal BMD values and content (Table IV).
      Table IVFetal/neonatal studies
      StudyPopulationCalcium source/dosageOutcomes
      Koo, 1999
      • Koo W.W.
      • Walters J.C.
      • Esterlitz J.
      • Levine R.J.
      • Bush A.J.
      • Sibai B.
      Maternal calcium supplementation and fetal bone mineralization.
      256 maternal/neonatal pairs, 22 weeks gestation to delivery2 g/day calcium carbonate supplementIncreased total-body and lumbar BMC in infant correlated with increased total maternal calcium intake
      Raman, 1978
      • Raman L.
      • Rajalakshmi K.
      • Krishnamachari K.A.
      • Sastry J.G.
      Effect of calcium supplementation to undernourished mothers during pregnancy on the bone density of the bone density of the neonates.
      87 maternal/neonatal pairs, 20 weeks gestation to deliveryGroup 1: no supplementMaternal BMD increase in 4th metacarpal in Group 3
      Group 2: 300 mg/day calcium lactate supplementNeonatal BMD higher at ulna, radius, tibia, and fibula in Groups 2 & 3 than Group 1
      Group 3: 600 mg/day calcium lactate supplementHighest neonatal fibula BMD in Group 3
      Chang, 2003
      • Chang S.C.
      • O'Brien K.O.
      • Nathanson M.S.
      • Caulfield L.E.
      • Mancini J.
      • Witter F.R.
      Fetal femur length is influenced by maternal dairy intake in pregnant African American adolescents.
      350 African-American maternal/neonatal pairs, 20-34 weeks gestation to 42 weeks postpartumDietary calcium (dairy)Positive correlation between maternal dairy intake and fetal femur length
      Half of population consumed <600mg/day
      Krishnamachari and Iyengar, 1975
      • Krishnamachari K.A.
      • Iyengar L.
      Effect of maternal malnutrition on the bone density of the neonates.
      15 maternal/neonatal pairs from high socioeconomic group, 21 maternal/neonatal pairs from low socioeconomic groupDietary calciumNeonatal BMD at radius, ulna, tibia, and fibula higher in high socioeconomic group than low socioeconomic group
      Pregnant women at 22 weeks of gestation consumed a 2-g calcium carbonate supplement or a placebo daily to test the effects of supplementation on fetal BMC.
      • Koo W.W.
      • Walters J.C.
      • Esterlitz J.
      • Levine R.J.
      • Bush A.J.
      • Sibai B.
      Maternal calcium supplementation and fetal bone mineralization.
      For all subjects, there was a significant trend that indicated a positive association between total maternal calcium intake and mean total-body BMC and lumbar spine BMC in the fetus. Comparisons between the calcium and placebo groups demonstrated that neonates in the calcium group had a higher total-body BMC and lumbar spine BMC than those neonates in the group without supplementation. Essentially, this study concluded that a maternal calcium supplementation of approximately 1300 mg daily can enhance fetal bone mineralization in women with low calcium intakes, even in affluent countries.
      • Koo W.W.
      • Walters J.C.
      • Esterlitz J.
      • Levine R.J.
      • Bush A.J.
      • Sibai B.
      Maternal calcium supplementation and fetal bone mineralization.
      Raman et al
      • Raman L.
      • Rajalakshmi K.
      • Krishnamachari K.A.
      • Sastry J.G.
      Effect of calcium supplementation to undernourished mothers during pregnancy on the bone density of the bone density of the neonates.
      evaluated the effect of different strengths of a calcium supplement in 87 pregnant women from 20 weeks of gestation until delivery. The bone density of the neonates was tested to determine the effect of supplementation with 300-mg/d calcium lactate, 600-mg/d calcium lactate, or placebo. For both supplementation groups, a statistically higher neonatal BMD value was observed at all sites that were tested (ulna, radius, tibia, and fibula) compared with placebo. The only statistically significant difference between the 600-mg/d group and the 300-mg/d group appeared in an analysis of the fibula maternal BMD values. This study demonstrates that calcium supplementation in pregnant women results in an increased initial bone density of the neonate that is essential because bone density progressively increases with age, building on the initial levels.
      • Raman L.
      • Rajalakshmi K.
      • Krishnamachari K.A.
      • Sastry J.G.
      Effect of calcium supplementation to undernourished mothers during pregnancy on the bone density of the bone density of the neonates.
      Fetal femur length was examined as a function of maternal dairy consumption in a study of 350 pregnant black adolescents.
      • Chang S.C.
      • O'Brien K.O.
      • Nathanson M.S.
      • Caulfield L.E.
      • Mancini J.
      • Witter F.R.
      Fetal femur length is influenced by maternal dairy intake in pregnant African American adolescents.
      Dietary calcium intakes were divided by “servings” that were estimated to be approximately 300 mg each. One half of the study population consumed <600 mg/d, which is <50% of the recommended intake. A strong positive correlation between maternal dairy intake and fetal femur length, as determined by ultrasound examination, was observed. Although a high dairy intake was associated with an overall improved nutritional intake, nutrients other than calcium were found not to be confounding variables in the determination of fetal femur length, which suggests that a calcium supplement would provide comparable benefits to diet alone.
      Although it is important to note that data from developing nations should be interpreted with caution, because they may not be applicable necessarily to the western populations. Data from studies that were conducted in India and Gambia are included for completeness. As such, in a study in India, maternal malnutrition, which included calcium deficiency and its effect on fetal BMD values, was evaluated by comparing pregnant women of high and low socioeconomic communities, which was defined by their income.
      • Krishnamachari K.A.
      • Iyengar L.
      Effect of maternal malnutrition on the bone density of the neonates.
      Women in the upper socioeconomic group consumed 700 to 800 mg/d calcium, although members of the low socioeconomic group consumed only 300 mg/d calcium. Fetal BMD values at the radius, ulna, tibia, and fibula were significantly higher in the upper socioeconomic group than in the low socioeconomic group. Maternal BMD values followed a similar trend, with an increased BMD value in the high socioeconomic group compared with the low socioeconomic group at all sites.
      Another study that included women in Gambia has results that contrast with the previously cited studies in that they conclude that maternal bone changes during lactation are independent of calcium supplementation.
      • Prentice A.
      • Jarjou L.M.
      • Cole T.J.
      • Stirling D.M.
      • Dibba B.
      • Fairweather-Tait S.
      Calcium requirements of lactating Gambian mothers: effects of a calcium supplement on breast-milk calcium concentration, maternal bone mineral content, and urinary calcium excretion.
      • Fairweather-Tait S.
      • Prentice A.
      • Heumann K.G.
      • Jarjou L.M.
      • Stirling D.M.
      • Wharf S.G.
      Effect of calcium supplements and stage of lactation on the calcium absorption efficiency of lactating women accustomed to low calcium intakes.
      • Prentice A.
      Calcium requirements of breast-feeding mothers.
      • Prentice A.
      • Jarjou L.M.
      • Stirling D.M.
      • Buffenstein R.
      • Fairweather-Tait S.
      Biochemical markers of calcium and bone metabolism during 18 months of lactation in Gambian women accustomed to a low calcium intake and in those consuming a calcium supplement.
      Other studies have come to similar conclusions that eliminate maternal calcium intake as a predictor of bone density. Knowledge of calcium as a “threshold” nutrient, in that a certain amount of the nutrient is used and all excess is excreted, also raises the question of the efficacy of extreme supplementation. Some studies that detect a negative change in BMD values, despite supplementation, are based on subjects who consumed more than the recommended amount of calcium at baseline examinations.
      • Prentice A.
      Calcium requirements of breast-feeding mothers.
      Many studies also observed that the BMD values that were lost during pregnancy and that lactation is regained by the resumption of menses independent of calcium intake
      • Laskey M.A.
      • Prentice A.
      • Hanratty L.A.
      • Jarjou L.M.
      • Dibba B.
      • Beavan S.R.
      Bone changes after 3 mo of lactation: influence of calcium intake, breast-milk output, and vitamin D-receptor genotype.
      ; however, BMD value increase does not always restore BMD values to the level before pregnancy. The bone responds to other stresses throughout the lifespan by depleting bone mass and that loss and this loss can be countered by increased calcium consumption. It is a logical conclusion, which is supported by available literature, that a similar increase in calcium consumption during pregnancy and lactation would reduce the loss of bone mass during these specific periods.

      Heartburn symptom relief

      Because many women experience heartburn during their pregnancy, calcium-based antacids (such as calcium carbonate) can be used both for heartburn relief and as a calcium supplement to provide bone health benefits. Antacids are the preferred first-line defense for treating heartburn symptoms. They are used by 30% to 50% of pregnant women to control heartburn symptoms and are available in a variety of forms.
      • Lewis J.H.
      • Weingold A.B.
      The use of gastrointestinal drugs during pregnancy and lactation.
      Calcium antacids are safe for use during pregnancy and result in an 80% improvement in symptoms.
      • Tytgat G.N.
      • Heading R.C.
      • Muller-Lissner S.
      • Kamm M.A.
      • Scholmerich J.
      • Berstad A.
      Contemporary understanding and management of reflux and constipation in the general population and pregnancy: a consensus meeting.
      • Black R.A.
      • Hill D.A.
      Over-the-counter medications in pregnancy.
      Animal studies have not found any adverse effects from exposure to high doses of calcium carbonate before mating and during pregnancy,
      • Shackelford M.E.
      • Collins T.F.
      • Welsh J.J.
      • Black T.N.
      • Ames M.J.
      • Chi R.K.
      Foetal development in rats fed AIN-76A diets supplemented with excess calcium.
      nor have teratogenic effects been observed in human cases.

      Lilienthal D, Ormond K, Pergament E. Gastroesophageal reflux (GERD) medications in pregnancy. Accessed June 18, 2004. Available at: http://www.fetal-exposure.org/REFLUX.html.

      Nearly 25% of the women who were surveyed consumed >10% of the daily calcium requirement from calcium-containing antacids.
      • Harville E.W.
      • Schramm M.
      • Watt-Morse M.
      • Chantala K.
      • Anderson J.J.
      • Hertz-Picciotto I.
      Calcium intake during pregnancy among white and African-American pregnant women in the United States.
      Between 45% and 85% of pregnant women experience heartburn symptoms, and many of them use over-the-counter medications that are convenient and easy to use to abate the symptoms.
      • Broussard C.N.
      • Richter J.E.
      Treating gastro-oesophageal reflux disease during pregnancy and lactation: what are the safest therapy options?.
      A study of 607 pregnant women found that the prevalence and severity of heartburn, which afflicted 72% of the subjects by the third trimester, increased with gestational age.
      • Marrero J.M.
      • Goggin P.M.
      • de Caestecker J.S.
      • Pearce J.M.
      • Maxwell J.D.
      Determinants of pregnancy heartburn.
      The physical discomfort that was experienced by women with heartburn symptoms can negatively impact the nutritional quality of maternal diets, including calcium intake. Calcium-containing antacids are a valuable calcium source for those with a calcium deficit by providing a vehicle through which many can remedy their insufficient dietary calcium intake.
      The most common mechanism of heartburn relief is acid reduction; however, recently, chewable calcium-based antacids have been shown to improve lower esophageal sphincter pressure for >30 minutes, which can aid in heartburn relief.

      DeVault KR. Gastroesophageal reflux disease. Digest Disease Week 2003: Primary Care Focus. May 18-21, 2003, Orlando, FL.

      In addition, the calcium-based antacids improved the initiation of peristalsis and acid clearance.
      • Rodriguez-Stanley S.
      • Ahmed T.
      • Zubaidi S.
      • Riley S.
      • Miner Jr., P.B.
      Luminal calcium from chewable antacids improves esophageal function.
      These findings suggest that calcium, in the form of calcium carbonate, may play a pivotal role in smooth muscle function, which is essential during pregnancy to prevent symptoms and provide relief of heartburn.
      • Rodriguez-Stanley S.
      • Ahmed T.
      • Zubaidi S.
      • Riley S.
      • Miner Jr., P.B.
      Luminal calcium from chewable antacids improves esophageal function.
      On the basis of its benefits in reducing heartburn symptoms while contributing to maternal and fetal calcium stores, calcium carbonate antacids are both ideal and safe for use by pregnant women.

      Comment

      Calcium is an essential nutrient during pregnancy and lactation that supports the growth and development of the fetus, especially because of its maternal-fetal transfer. Pregnancy places a significant demand on calcium, in that the dynamic balance of calcium storage is upset, and calcium is drawn from the maternal skeleton. Because most pregnant women do not consume the recommended quantity of calcium at any time in their lives, including the critical pregnancy and lactation periods, supplementation should be recommended to restore the balance.
      Studies indicate that increases in calcium intake during pregnancy and lactation improve maternal bone health while also providing a larger source of calcium to the fetus. Adequate calcium consumption can replace lost maternal bone mass, reduce bone resorption, and, in some cases, reverse bone loss so that bone mass is gained. Calcium supplementation during pregnancy can be linked directly to increased bone density and bone length of neonates.
      In addition to maternal and fetal skeletal benefits of calcium supplementation, many other advantages have been linked to adequate calcium intake. Maternal health is maintained with a reduced risk of pregnancy-induced hypertension
      • Carroli G.
      • Duley L.
      • Belizan J.M.
      • Villar J.
      Calcium supplementation during pregnancy: a systematic review of randomised controlled trials.
      • Hofmeyr G.J.
      • Roodt A.
      • Atallah A.N.
      • Duley L.
      Calcium supplementation to prevent pre-eclampsia–a systematic review.
      • Villar J.
      • Belizan J.M.
      Same nutrient, different hypotheses: disparities in trials of calcium supplementation during pregnancy.
      and a decrease in circulating lead.
      • Gulson B.L.
      • Mahaffey K.R.
      • Jameson C.W.
      • Mizon K.J.
      • Korsch M.J.
      • Cameron M.A.
      Mobilization of lead from the skeleton during the postnatal period is larger than during pregnancy.
      • Lagerkvist B.J.
      • Ekesrydh S.
      • Englyst V.
      • Nordberg G.F.
      • Soderberg H.A.
      • Wiklund D.E.
      Increased blood lead and decreased calcium levels during pregnancy: a prospective study of Swedish women living near a smelter.
      Again, because of the exchange of maternal and fetal nutrients, numerous other benefits to fetal health have been observed. Higher birth weight babies,
      • Hofmeyr G.J.
      • Roodt A.
      • Atallah A.N.
      • Duley L.
      Calcium supplementation to prevent pre-eclampsia–a systematic review.
      • Yang C.Y.
      • Chiu H.F.
      • Chang C.C.
      • Wu T.N.
      • Sung F.C.
      Association of very low birth weight with calcium levels in drinking water.
      a reduced risk of preterm delivery,
      • Carroli G.
      • Duley L.
      • Belizan J.M.
      • Villar J.
      Calcium supplementation during pregnancy: a systematic review of randomised controlled trials.
      • Hofmeyr G.J.
      • Roodt A.
      • Atallah A.N.
      • Duley L.
      Calcium supplementation to prevent pre-eclampsia–a systematic review.
      • Crowther C.A.
      • Hiller J.E.
      • Pridmore B.
      • Bryce R.
      • Duggan P.
      • Hague W.M.
      Calcium supplementation in nulliparous women for the prevention of pregnancy-induced hypertension, preeclampsia and preterm birth: an Australian randomized trial: FRACOG and the ACT Study Group.
      decreased fetal lead exposure,
      • Gulson B.L.
      • Mahaffey K.R.
      • Jameson C.W.
      • Mizon K.J.
      • Korsch M.J.
      • Cameron M.A.
      Mobilization of lead from the skeleton during the postnatal period is larger than during pregnancy.
      • Crowther C.A.
      • Hiller J.E.
      • Pridmore B.
      • Bryce R.
      • Duggan P.
      • Hague W.M.
      Calcium supplementation in nulliparous women for the prevention of pregnancy-induced hypertension, preeclampsia and preterm birth: an Australian randomized trial: FRACOG and the ACT Study Group.
      and lower infant blood pressure
      • Hofmeyr G.J.
      • Roodt A.
      • Atallah A.N.
      • Duley L.
      Calcium supplementation to prevent pre-eclampsia–a systematic review.
      • Hatton D.C.
      • Harrison-Hohner J.
      • Coste S.
      • Reller M.
      • McCarron D.
      Gestational calcium supplementation and blood pressure in the offspring.
      • Belizan J.M.
      • Villar J.
      • Bergel E.
      • del Pino A.
      • Di Fulvio S.
      • Galliano S.V.
      Long-term effect of calcium supplementation during pregnancy on the blood pressure of offspring: follow up of a randomised controlled trial.
      have all been linked with a high calcium intake during pregnancy.
      Also, it has been shown that calcium supplementation during pregnancy can reduce the incidence of preeclampsia. These reduced rates of preeclampsia (a serious condition with maternal and fetal complications) also have been associated with proper calcium consumption in women with low calcium intake. This condition is a major cause of maternal morbidity and death and a contributor to preterm delivery, intrauterine growth restriction, and perinatal death.
      • Morris C.D.
      • Jacobson S.L.
      • Anand R.
      • Ewell M.G.
      • Hauth J.C.
      • Curet L.B.
      • et al.
      Nutrient intake and hypertensive disorders of pregnancy: Evidence from a large prospective cohort.
      Calcium consumption during pregnancy can lead to a 45% to 75% reduction in the incidence of preeclampsia.
      • Yang C.Y.
      • Chiu H.F.
      • Chang C.C.
      • Wu T.N.
      • Sung F.C.
      Association of very low birth weight with calcium levels in drinking water.
      In the National Institutes of Health trial entitled “Calcium for the Prevention of Preeclampsia,” patients received 2000 mg of calcium carbonate daily; preeclampsia was seen in 6.9% of the calcium group as compared with 7.3% of the placebo group.
      • Levine R.J.
      • Hauth J.C.
      • Curet L.B.
      • Sibai B.M.
      • Catalano P.M.
      • Morris C.D.
      • et al.
      Trial of calcium to prevent preeclampsia.
      Other studies have seen similar and more substantial preeclampsia-lowering effects of calcium in doses that range from 1000 mg to 2000 mg daily.
      • Carroli G.
      • Duley L.
      • Belizan J.M.
      • Villar J.
      Calcium supplementation during pregnancy: a systematic review of randomised controlled trials.
      • Hofmeyr G.J.
      • Roodt A.
      • Atallah A.N.
      • Duley L.
      Calcium supplementation to prevent pre-eclampsia: a systematic review.
      Although most of the data suggest a beneficial effect of calcium supplementation, the variation between studies regarding locations of measurements, reporting methods, and small sample sizes in some studies would make a quantitative comparison of the data extremely complex. Similarly, in many of the studies, improvements in bone health were not universal for all tested bone sites. Although the beneficial effects were not perceived at all sites, the overall trend indicates a positive correlation between calcium supplementation and bone health. Different studies use a variety of reporting methods, such as BMD scans, calculations of BMC, ultrasound examinations, and collagen and hormonal levels. Ethical restrictions on clinical trials regarding supplementation during pregnancy reduce the availability of studies.
      Pregnant women who consume low-calcium diets have the most to gain from a calcium supplement as they enter a period of calcium imbalance with an already depleted skeleton, which leads to the extraction of calcium from maternal stores to meet fetal developmental needs.
      • Prentice A.
      Maternal calcium metabolism and bone mineral status.
      An efficient method of obtaining this increased calcium load is through calcium-containing antacids, which provide the dual benefits of short-term heartburn symptom relief and long-term preservation and/or creation of maternal and fetal bone mass. Based on the studies that we examined, increased calcium intake during pregnancy and lactation, especially through supplementation, can result in meaningful public health improvements that benefit both maternal and fetal skeletal health.

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