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REVIEW ARTICLE
KEY WORDS
Calcium
Pregnancy
Lactation
Fetal
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.
2006 Mosby, Inc. All rights reserved.
938
Table I
Food source
Low-fat plain yogurt
Low-fat yogurt with fruit
Sardines
Cheddar cheese, shredded
Skim milk
2% Low-fat milk
Whole milk
Buttermilk
Mozzarella, part skim
Tofu, firm
Orange juice, calcium
fortified
Salmon with bones
Pudding, chocolate w/2%
milk
Cottage cheese 1% milk fat
Tofu, soft
Spinach, cooked
Frozen yogurt, vanilla,
soft serve
Turnip greens, boiled
Kale, cooked
Kale, raw
Ice cream, vanilla
Bread, white
Broccoli, raw
Table II
Serving
size (oz)
Calcium content
per serving (mg)
8
8
3
1.5
8
8
8
8
1.5
4
6
415
245-384
324
306
302
297
291
285
275
205
200-260
3
4
181
153
8
4
4
4
138
138
120
103
4
8
8
4
1
4
99
94
90
85
31
21
Age (years)
Adequate
Daily intakes
(mg/day)
Mean
Daily intake
(mg/day)
14-18
19-39
1300
1000
793
797
Adapted from the DRI reports at the USDA Food and Nutrition
Information Center, 2004 and Ervin, 2004.
939
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.10,24,25 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.26 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,27
O5% 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.28 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.21 Therefore, adequate calcium consumption is vital, especially for pregnant and lactating women.
Pregnancy
A wealth of information exists to indicate that increased
calcium intake and calcium supplementation improves
bone health throughout the lifespan.29-31 Yet, there are
limited studies regarding the eect of supplementation
during pregnancy because of medical/legal/ethical concerns (Table III). Janakiraman et al23 published 1 of the
rst papers to examine the eect of calcium supplementation during pregnancy on the rates of maternal bone
resorption.
940
Table III
Study
Calcium source/dosage
Outcomes
Janakiraman, 200323
Population
Cross, 199534
31 pregnant Mexican
women, 25 to 35
weeks gestation
Baseline to
15 lactating women,
lactation
2 weeks postpartum
to 3 months lactation
Lactation to
15 lactating women, 3
postweaning
months lactation to
3 months post-weaning
Lactation
One study examined BMD values as a function of
dietary calcium intake, which demonstrated evidence for
the benets of calcium during lactation.32 Twenty-six
lactating women and 8 nonlactating women were observed for the eect of dietary calcium intake on maternal
BMD values from delivery until 7 months after delivery. In
941
Fetal/neonatal studies
Study
Population
Koo, 199936
Calcium source/dosage
Outcomes
Postweaning phase
In the postweaning phase, Cross et al34 demonstrated
the benecial eects of calcium carbonate supplementation. The calcium group signicantly increased BMD
values at the lumbar region 3%; the placebo groups
increase did not reach statistical signicance. Signicant
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 signicant
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,35 signicant 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 signicantly 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.
942
eect 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 bula) compared with placebo. The
only statistically signicant dierence between the 600mg/d group and the 300-mg/d group appeared in an
analysis of the bula 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.37
Fetal femur length was examined as a function of
maternal dairy consumption in a study of 350 pregnant
black adolescents.14 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
benets 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 deciency and its
eect on fetal BMD values, was evaluated by comparing
pregnant women of high and low socioeconomic communities, which was dened by their income.38 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 bula were
signicantly 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.12,39-41 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 ecacy of extreme supplementation.
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 signicant 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 benets of
calcium supplementation, many other advantages have
been linked to adequate calcium intake. Maternal health
is maintained with a reduced risk of pregnancy-induced
hypertension52-54 and a decrease in circulating lead.55,56
Again, because of the exchange of maternal and fetal
nutrients, numerous other benets to fetal health have
been observed. Higher birth weight babies,53,57 a reduced
risk of preterm delivery,52,53,58 decreased fetal lead exposure,55,58 and lower infant blood pressure53,59,60 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.61 Calcium consumption
during pregnancy can lead to a 45% to 75% reduction in
the incidence of preeclampsia.57 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
943
group.62 Other studies have seen similar and more
substantial preeclampsia-lowering eects of calcium in
doses that range from 1000 mg to 2000 mg daily.52,63
Although most of the data suggest a benecial eect 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 benecial eects 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.22 An
ecient method of obtaining this increased calcium load
is through calcium-containing antacids, which provide
the dual benets 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
benet both maternal and fetal skeletal health.
References
1. Institute of Medicine. DRI dietary reference intakes for calcium,
phosphorus, magnesium, vitamin D, and uoride. Washington
(DC): National Academy Press; 1997.
2. Prentice A. Calcium in pregnancy and lactation. Annu Rev Nutr
2000;20:249-72.
3. Heaney RP. Calcium, dairy products and osteoporosis. J Am Coll
Nutr 2000;19(suppl):83S-99S.
4. Tresolini CP, Gold DT, Lee LS. Working with patients to prevent,
treat, and manage osteoporosis: a curriculum guide for the health
professions. 3 ed. San Francisco, CA: National Fund for Medical
Education; 2001.
5. US Department of Health and Human Services. Report of the
Surgeon Generals 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.
6. Wallace K, Baron JA, Cole BF, Sandler RS, Karagas MR, Beach
MA, et al. Eect of calcium supplementation on the risk of large
bowel polyps. J Natl Cancer Inst 2004;96:921-5.
7. US Department of Health and Human Services, Health Resources
and Services Administration Maternal and Child Health Bureau.
Womens health USA 2003. Rockville (MD): US Department of
Health and Human Services; 2003.
8. US Department of Agriculture, Agricultural Research Service.
Results from USDAs 1994-1996 diet and health knowledge
944
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
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.
Ervin RB, Wang CY, Wright JD, Kennedy-Stephenson J. Dietary
intake of selected minerals for the United States population: 19992000: advance data from vital and health statistics; no. 341.
Hyattsville (MD): National Center for Health Statistics; 2004.
Drinkwater BL, Chesnut CH 3rd. Bone density changes during
pregnancy and lactation in active women: a longitudinal study.
Bone Miner 1991;14:153-60.
Givens MH, Macy IG. The chemical composition of the human
fetus. J Biol Chem 1933;102:7-17.
Prentice A, Jarjou LM, Cole TJ, Stirling DM, Dibba B, Fairweather-Tait S. Calcium requirements of lactating Gambian
mothers: eects of a calcium supplement on breast-milk calcium
concentration, maternal bone mineral content, and urinary calcium excretion. Am J Clin Nutr 1995;62:58-67.
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.
Chang SC, OBrien KO, Nathanson MS, Cauleld LE, Mancini J,
Witter FR. Fetal femur length is inuenced by maternal dairy
intake in pregnant African American adolescents. Am J Clin Nutr
2003;77:1248-54.
Harville EW, Schramm M, Watt-Morse M, Chantala K, Anderson
JJ, Hertz-Picciotto I. Calcium intake during pregnancy among
white and African-American pregnant women in the United States.
J Am Coll Nutr 2004;23:43-50.
US Department of Agriculture, Center for Nutrition Policy and
Promotion. Federal Studies. Review of the nutritional status of
WIC participants. Fam Econ Nutr Rev 2001;13:118-9.
Frank E, Cone K. Characteristics of pregnant vs. non-pregnant
women physicians: ndings from the women physicians health
study. Int J Gynaecol Obstet 2000;69:37-46.
Frank E, Breyan J, Elon L. Physician disclosure of healthy
personal behaviors improves credibility and ability to motivate.
Arch Fam Med 2000;9:287-90.
Frank E, Rothenberg R, Lewis C, Belodo BF. Correlates of
physicians prevention-related practices: ndings from the Women
Physicians Health study. Arch Fam Med 2000;9:359-67.
Putnam JJ, Allshouse JE. Food consumption, prices, and expenditures, 1970-97: statistical bulletin no. 965. Washington (DC):
Food and Rural Economics Division, Economic Research Service,
US Department of Agriculture; 1999.
Kalkwarf HJ, Specker BL. Bone mineral changes during pregnancy and lactation. Endocrine 2002;17:49-53.
Prentice A. Maternal calcium metabolism and bone mineral status.
Am J Clin Nutr 2000;71(suppl):1312S-6S.
Janakiraman V, Ettinger A, Mercado-Garcia A, Hu H, HernandezAvila M. Calcium supplements and bone resorption in pregnancy:
a randomized crossover trial. Am J Prev Med 2003;24:260-4.
Anito P, Tommaselli GA, di Carlo C, Guida F, Nappi C.
Changes in bone mineral density and calcium metabolism in
breastfeeding women: a one year follow-up study. J Clin Endocrinol Metab 1996;81:2314-8.
Kent GN, Price RI, Gutteridge DH, Allen JR, Rosman KJ, Smith
M. Eect of pregnancy and lactation on maternal bone mass and
calcium metabolism. Osteoporos Int 1993;3(suppl):44-7.
Sowers MF, Scholl T, Harris L, Jannausch M. Bone loss in adolescent and adult pregnant women. Obstet Gynecol 2000;96:189-93.
Pearson D, Kaur M, San P, Lawson N, Baker P, Hosking D.
Recovery of pregnancy mediated bone loss during lactation. Bone
2004;34:570-8.
Naylor KE, Iqbal P, Fledelius C, Fraser RB, Eastell R. The eect
of pregnancy on bone density and bone turnover. J Bone Miner
Res 2000;15:129-37.
945
57. Yang CY, Chiu HF, Chang CC, Wu TN, Sung FC. Association of
very low birth weight with calcium levels in drinking water.
Environ Res 2002;89:189-94.
58. Crowther CA, Hiller JE, Pridmore B, Bryce R, Duggan P, Hague
WM. 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. Aust N Z J Obstet Gynaecol 1999;39:12-8.
59. Hatton DC, Harrison-Hohner J, Coste S, Reller M, McCarron D.
Gestational calcium supplementation and blood pressure in the
ospring. Am J Hypertens 2003;16:801-5.
60. Belizan JM, Villar J, Bergel E, del Pino A, Di Fulvio S, Galliano
SV. Long-term eect of calcium supplementation during pregnancy on the blood pressure of ospring: follow up of a
randomised controlled trial. BMJ 1997;315:281-5.
61. Morris CD, Jacobson SL, Anand R, Ewell MG, Hauth JC, Curet
LB, et al. Nutrient intake and hypertensive disorders of pregnancy:
Evidence from a large prospective cohort. Am J Obstet Gynecol
2001;184:643-51.
62. Levine RJ, Hauth JC, Curet LB, Sibai BM, Catalano PM, Morris
CD, et al. Trial of calcium to prevent preeclampsia. N Engl J Med
1997;337:69-76.
63. Hofmeyr GJ, Roodt A, Atallah AN, Duley L. Calcium supplementation to prevent pre-eclampsia: a systematic review. S Afr
Med J 2003;93:224-8.
64. Kalkwarf HJ, Specker BL, Bianchi DC, Ranz J, Ho M. The eect
of calcium supplementation of bone density during lactation after
weaning. N Engl J Med 1997;337:523-8.