Pregnancy is a remarkable and challenging time for the adolescent mother and the fetus. For the adolescent mother, pregnancy places a stress on the calcium (Ca) needs of her growing and maturing skeleton, because the adolescent growth spurt is not complete until a few years after menarche.1 The recommended adequate intake for Ca during pregnancy is 1,300 mg daily, which is the highest during a woman’s lifetime.2
Fetal Ca accretion is the foundation of the highest Ca accretion in one’s lifetime. Bone mass accretion during the first year of life is greater than that achieved at any other stage of life, including adolescence.3 Optimizing Ca and bone status in the fetus may provide long-term benefits by helping infants program their skeletal growth to reach their maximal genetic potential for peak bone mass, a prerequisite for the prevention of osteoporosis and fractures.4,5
In the United States, dairy products are the major contributors of Ca in the typical diet.6 However, pregnant adolescents are consuming less milk and more snack foods than adult pregnant mothers.7 There are other alternative Ca sources, such as Ca fortified orange juices (orange juice plus calcium), that can contribute Ca to the diet of the pregnant adolescent. The purpose of this study is to evaluate the effects of dietary Ca intervention on adolescent pregnant mothers and their newborn from two different food sources, dairy and orange juice plus calcium.
PARTICIPANTS AND METHODS
Seventy-two healthy pregnant adolescent mothers aged 15–17 years were recruited from our University of Utah Teen Mother and Child Program and from private obstetric practices. Mothers excluded from this study included those with hypertension, diabetes, renal or liver diseases, and those who used alcohol, tobacco, or medications that would affect Ca metabolism during the pregnancy. All mothers were enrolled before 20 weeks of gestation as determined by the mother’s last normal menstrual period. Pregnancy dating was confirmed with ultrasound. Enrollment occurred during a 15-month period. All mothers were primiparous except for one.
Pregnant mothers were randomly assigned to one of three groups: control, orange juice fortified with calcium, and dairy. Computer-generated randomization was kept in sealed envelopes. The control group consumed their usual diet while the orange juice plus calcium group were counseled to consume at least four servings of orange juice plus calcium (more than 1,200 mg Ca) so that their Ca intake would be similar to the dairy group. The dairy group was counseled to consume at least four servings of dairy products (more than 1,200 mg Ca) daily. Dairy products consist of milk, yogurt, and cheese. All mothers were counseled on proper nutrition during pregnancy.
At enrollment, 6 months, and delivery, maternal weight, height, blood pressure (BP) and 2-day dietary record were taken. Randomized and unscheduled 24- hour dietary recalls were included to evaluate compliance to the diets. At delivery, mother’s blood was drawn for serum Ca, phosphate (P), magnesium (Mg), zinc (Zn), 25-hydroxvitamin D (D), total protein, vitamin A, folate, and vitamin B12 levels. At delivery, the newborn infant’s birth weight, length, head circumference, and BP were recorded as well as total body composition for bone mineral Ca, fat, and lean mass as determined by dual energy X-ray absorptiometry scan. Umbilical blood was also collected for serum Ca, D, and total protein levels. The University of Utah Institutional Board Review approved this study and all mothers gave informed consent.
Dietary records were analyzed for total calories, Ca, P, protein, fats, and vitamins by a computer software dietary program based on U.S. Department of Agriculture handbooks and tables (Nutritrac, Mosby, Los Angeles, CA). Dietary compliance for both the orange juice plus calcium and dairy groups was expected to meet the minimal requirements of four servings of the orange juice plus calcium or the dairy products. Compliance was monitored by weekly monitoring of the dietary intakes of the mothers and unscheduled dietary recalls. However, the protocol was changed actively when the mothers in the orange juice plus calcium group could not comply with consuming the four servings of orange juice and calcium. Calcium carbonate tablets were added to the mothers in the orange juice plus calcium group so that their intake would meet the daily Ca requirement of 1,200 mg and be similar to the dairy group.
Serum Ca, Mg, and Zn were determined by atomic absorptiometry. Serum P levels were assayed using the method of Fiske and Subbarow using the colorimetric method.8 The radioimmuno competitive protein binding assay determined 25-hydroxyvitamin D levels.9 Vitamin B12 and folate levels were assayed using the radioassay dual isotope method.10 Serum total protein level was determined by the improved biuret colorimetric method. Vitamin A determinations were done by the fluorometric micromethod.11
Dual energy X-ray absorptiometry (DXA) was the method used to determine the infant total body composition (XR-36 system, Norland Corporation, Fort Atkinson, WI). The accuracy of this method is less than 2% error for bones, fat, and lean mass.12–14
Frequency variables between the groups were analyzed using the χ2 analyses. Differences in weight, height, and BP among the mothers were tested by repeated measures analyses of variance. Dietary intakes of the various nutrients among the three groups were compared by repeated measures analyses of variance at each period. Multiple comparison posttests were performed using the Tukey analyses. By separation of gender, differences in infant’s weight, height, head circumference, BP, and body composition values among the three groups were determined by Student t tests. Values of P<.01 were considered significant.
Sample size calculation was based on the results of birth weight gains in infants whose mothers were taking Sustacal (Mead Johnson Nutritionals, Bristol Myers Squibb, Evansville, IN).15 Assuming a difference of 300 g in birth weights with a standard deviation of 500 g, the calculated sample size is 22 in each group for a proposed alpha of 0.05 and a power of 0.80.
The flow of subjects is presented in Figure 1. At start of the study (mean gestation of 18 weeks), 6 months, and at delivery (mean gestation of 39 weeks), all mothers were similar in weight, height, and BP (Table 1). Dietary intakes during the pregnancy are shown in Tables 2 and 3. One half of the mothers in the orange juice plus calcium group failed to meet the necessary intake of four servings of orange juice because of gastrointestinal intolerance to the orange juice. These mothers were taking two or three servings of the orange juice and Ca carbonate supplement was added to meet the required Ca intake of 1,200 mg daily. There were no differences between the mothers taking at least the four servings of the orange juice plus calcium and those mothers taking the Ca supplement with the orange juice plus calcium in regard to maternal dietary intakes, weight, height, BP, or newborn values.
There were differences in Ca, P, vitamin D, riboflavin, Zn, and iron among the three groups at 6 months and delivery. The randomized, unscheduled 24-hour recalls were similar to the dietary records at 6 months and delivery. Most of the mothers in the dairy group were consuming 2% milk as their dairy product.
Maternal blood values are shown in Table 4. There were differences in folate, P, and D levels among the three groups. All values were within the normal adult range.
The birth weights of the infants in the dairy group (3,517±273 g) were heavier than the birth weights of the infants in the control (3,277±177 g) and orange juice plus calcium (3,292±165 g) groups, P<.001. There were no differences in weight between infants in the control and orange juice plus calcium groups. All infants had similar length, head circumference, and BP. The gender distribution was similar among the three groups: 10 females and 13 males in the controls, 14 females and 10 males in the orange juice plus calcium group, and 13 females and 12 males in the dairy group.
The infants in the dairy group had higher total body Ca than infants in the control group (Fig. 2). There was no difference in total body Ca between infants in the dairy group and the orange juice plus calcium group. Also, there was no difference in total body Ca in the orange juice plus calcium group and the control group. Lean and fat mass as measured by DXA was similar among the three groups. Lean mass for control was 2,434±356 g, 2,510±248 g for infants in the orange juice plus calcium group, and 2,554±326 g for infants in the dairy group. Fat mass for control infants was 809±318 g, 817±316 g for infants in the orange juice plus calcium group, and 926±306 g for infants in the dairy group. Blood pressures among the three groups were also similar.
The D levels were higher in the dairy group than in the control and orange juice plus calcium groups. Total protein and Ca levels were similar among the three groups.
Calcium is an important mineral during pregnancy. Calcium supplementation during pregnancy is associated with maternal bone mineralization,16 lower BP,17 and reduction of preterm deliveries.18 In our study, diet supplement with dairy products during adolescent pregnancy increased the cord blood 25-hydroxyvitamin D levels and the newborn birth weight and total body Ca without increases in lean or fat mass. Calcium diet supplemented with dairy products improved the mothers’ diet without affecting their weight, height, or BP during pregnancy. In this study we evaluated Ca supplementation by dairy products or orange juice plus calcium. Only the adolescent mothers on dairy products had the heavier newborn compared with controls and mothers on orange juice plus calcium.
In the consumption of dairy foods, it is difficult to determine which nutrient or combination of nutrients was responsible for the infant’s gain in birth weight and total body Ca. However, the intake of dairy products increased the vitamin D intake over the other two groups. Dairy foods are the only food products fortified with vitamin D. The higher 25- hydroxyvitamin D levels in the mother and cord reflect the increased vitamin D intake by the mothers. We speculate that the higher Ca and vitamin D intakes promoted the higher fetal Ca accretion.
Maternal weight gain seems to be an important factor in newborn outcome.19 In adolescent pregnancy, low or inadequate weight gain (less than 4.3 kg by 24 weeks of gestation) is associated with preterm delivery.20 Protein and energy supplementations in normal pregnant women have shown no effect on the newborn’s birth weight.21,22 However, nutritional supplementation in pregnant women who have marginal dietary status has resulted in higher maternal weight gain, improved newborn birth weight, and decreased prevalence of low birth weight infants.23–27 In our study, all three groups had similar and adequate dietary intakes of calories, proteins, and fats with normal maternal weight gains during pregnancy.
A study of nutritional supplementation in 78 disadvantaged pregnant black adolescents demonstrated a positive effect on their newborns. These adolescents received daily 240 mL of Sustacal that contained 240 mg Ca, 240 kcal, 14.5 g protein, and 5.6 g of fat for about 15 weeks. The supplemented group infants’ birth weights were 269 g higher than the controls, 3,115±499 compared with 2,958±514 g.15
A high Ca intake (1,575 mg/day) from dairy products during the first 20 weeks of pregnancy was associated with a low risk of gestational hypertension. The association was independent of body mass index, exercise, maternal age, education, and cigarette smoking.28 Maternal Ca supplementation of 2 g/d of elemental Ca during the second and third trimester can increase fetal total body bone mineralization by 15% in women with low dietary Ca intake of less than 600 mg/d.29 In our study, pregnant adolescent mothers who consumed dairy products had an average of 1,770 mg Ca daily and increased their fetal total body bone mineralization by 17% compared with controls who were ingesting 860 mg daily. The mothers on orange juice plus calcium ingested an average of 1,470 mg Ca daily and increased their fetal bone mineralization by 10% compare to the controls, but this was not significant.
Other Ca sources besides dairy products are orange juice plus calcium and vegetables. Orange juice fortified with Ca has similar Ca bioavailability as Ca carbonate supplements.30 However, the bioavailability of Ca from plant sources is hindered by the plant’s oxalates. In our study, the orange juice created gastrointestinal intolerance in one half of our subjects.
Maternal vitamin D intakes were higher in the dairy supplemented mothers compared with the other two groups, reflecting vitamin D content in dairy foods. It is not surprising that the vitamin D intake is low in the other two groups when dairy consumption is limited. Maternal vitamin D intakes during pregnancy were reflected in the higher umbilical cord vitamin D levels. This higher vitamin D with higher Ca intake in the fetus may have improved the intrauterine bone mineralization. Early programming of the fetal bone mineralization may be an important contributor for the prevention of adult osteoporotic fractures.31,32
In our study, the mothers receiving dairy supplements had higher serum folate levels compared with the other two groups. This finding may be clinically significant, because adequate folate nutrition is important in preventing neural tube defects in the fetus during pregnancy. Neural tube defects seem to be associated with younger mothers and with low dairy food intake.33 Several studies from animals34,35 and humans36,37 have suggested that the inclusion of milk in the diet enhances the bioavailability of folate. In summary, a diet supplemented with dairy products during adolescent pregnancy resulted in higher maternal vitamin D and folate serum levels and higher newborn weight and bone mineralization compared with controls.
1. Lenders CM, McElrath TF, Scholl TO. Nutrition in adolescent pregnancy. Curr Opin Pediatr 2000 Jun;12:291–6.
2. Standing committee on the scientific evaluation of dietary reference intakes, Food and Nutrition Board, Institute of Medicine. Dietary reference for calcium, phosphorus, magnesium, vitamin D and fluoride. Washington (DC): The National Academies Press; 1997.
3. Koo WW, Warren L. Calcium and bone health in infants. Neonatal Netw 2003;22:23–37.
4. Antoniades L, MacGregor AJ, Andrew T, Spector TD. Association of birth weight with osteoporosis and osteoarthritis in adult twins. Rheumatology (Oxford) 2003;42:791–6.
5. Sayer AA, Cooper C. Fetal programming of body composition and musculoskeletal development. Early Hum Dev 2005;81:735–44.
6. Subar AF, Krebs-Smith SM, Cook A, Kahle LL. Dietary sources of nutrients among US adults, 1989 to 1991. J Am Diet Assoc 1998;98:537–47.
7. Endres J, Dunning S, Poon SW, Welch P, Duncan H. Older pregnant women and adolescents: nutrition data after enrollment in WIC. J Am Diet Assoc 1987;87:1011–6, 1019.
8. Sauberlich HE. Laboratory tests for the assessment of nutritional status. Second edition. Boca Raton (FL): CRC Press; 1999.
9. Haddad JG, Chyu KJ. Competitive protein-binding radioassay for 25-hydroxycholecalciferol. J Clin Endocrinol Metab 1971;33:992–5.
10. Gutcho S, Mansbach L. Simultaneous radioassay of serum vitamin B12 and folic acid. Clin Chem 1977;23:1609–14.
11. Taylor SL, Lamden MP, Tappel AL. Sensitive fluorometric method for tissue tocopherol analysis. Lipids 1976;11:530–8.
12. Chan GM. Performance of dual-energy x-ray absorptiometry in evaluating bone, lean body mass, and fat in pediatric subjects. J Bone Miner Res 1992;7:369–74.
13. Koo WW, Walters J, Bush AJ, Chesney RW, Carlson SE. Dual-energy X-ray absorptiometry studies of bone mineral status in newborn infants. J Bone Miner Res 1996;11:997–1002.
14. Hammami M, Picaud JC, Fusch C, Hockman EM, Rigo J, Koo WW. Phantoms for cross-calibration of dual energy X-ray absorptiometry measurements in infants. J Am Coll Nutr 2002;21:328–32.
15. Paige DM, Cordano A, Mellits ED, Baertl JM, Davis L. Nutritional supplementation of pregnant adolescents. J Adolesc Health Care 1981;1:261–7.
16. Prentice A. Maternal calcium metabolism and bone mineral status. Am J Clin Nutr 2000;71:1312S–6S.
17. Atallah AN, Hofmeyr GJ, Duley L. Calcium supplementation during pregnancy for preventing hypertensive disorders and related problems. Cochrane Database Syst Rev 2002;(1):CD001059.
18. Villar J, Repke JT. Calcium supplementation during pregnancy may reduce preterm delivery in high-risk populations. Am J Obstet Gynecol 1990;163:1124–31.
19. Gutierrez Y, King JC. Nutrition during teenage pregnancy. Pediatr Ann 1993;22:99–108.
20. Kardjati S, Kusin JA, De With C. Energy supplementation in the last trimester of pregnancy in East Java: I. Effect on birthweight. Br J Obstet Gynaecol 1988;95:783–94.
21. Rush D, Stein Z, Susser M. A randomized controlled trial of prenatal nutritional supplementation in New York City. Pediatrics 1980;65:683–97.
22. Kramer MS, Kakuma R. Energy and protein intake in pregnancy. Cochrane Database Syst Rev 2003; (4):CD000032.
23. Lechtig A, Yarbrough C, Delgado H, Habicht JP, Martorell R, Klein RE. Influence of maternal nutrition on birth weight. Am J Clin Nutr 1975;28:1223–33.
24. Prentice AM, Cole TJ, Foord FA, Lamb WH, Whitehead RG. Increased birthweight after prenatal dietary supplementation of rural African women. Am J Clin Nutr 1987;46:912–25.
25. Begum N, Hussain T, Afridi B, Hamid A. Effect of supplementary feeding of pregnant women on birth weight of the new born. Plant Foods Hum Nutr 1991;41:329–36.
26. Ceesay SM, Prentice AM, Cole TJ, Foord F, Weaver LT, Poskitt EM, et al. Effects on birth weight and perinatal mortality of maternal dietary supplements in rural Gambia: 5 year randomised controlled trial [published erratum appears in BMJ 1997;315:1141]. BMJ 1997;315:786–90.
27. Van Eyk N, Allen LM, Sermer M, Davis VJ. Obstetric outcome of adolescent pregnancies. J Pediatr Adolesc Gynecol 2000;13:96.
28. Marcoux S, Brisson J, Fabia J. Calcium intake from dairy products and supplements and the risks of preeclampsia and gestational hypertension. Am J Epidemiol 1991;133:1266–72.
29. Koo WW, Walters JC, Esterlitz J, Levine RJ, Bush AJ, Sibai B. Maternal calcium supplementation and fetal bone mineralization. Obstet Gynecol 1999;94:577–82.
30. Martini L, Wood RJ. Relative bioavailability of calcium-rich dietary sources in the elderly. Am J Clin Nutr 2002;76:1345–50.
31. Dennison EM, Arden NK, Keen RW, Syddall H, Day IN, Spector TD, et al. Birthweight, vitamin D receptor genotype and the programming of osteoporosis. Paediatr Perinat Epidemiol 2001;15:211–9.
32. Cooper C, Javaid K, Westlake S, Harvey N, Dennison E. Developmental origins of osteoporotic fracture: the role of maternal vitamin D insufficiency. J Nutr 2005;135:2728S–34S.
33. Friel JK, Frecker M, Fraser FC. Nutritional patterns of mothers of children with neural tube defects in Newfoundland. Am J Med Genet 1995;55:195–9.
34. Colman N, Hettiarachchy N, Herbert V. Detection of a milk factor that facilitates folate uptake by intestinal cells. Science 1981;211:1427–9.
35. Mason JB, Selhub J. Folate-binding protein and the absorption of folic acid in the small intestine of the suckling rat. Am J Clin Nutr 1988;48:620–5.
36. Smith AM, Picciano MF, Deering RH. Folate intake and blood concentrations of term infants. Am J Clin Nutr 1985;41:590–8.
37. Picciano MF, West SG, Ruch AL, Kris-Etherton PM, Zhao G, et al. Effect of cow milk on food folate bioavailability in young women. Am J Clin Nutr 2004;80:1565–9.