Nutrition in Pregnancy
Harriet S. Salzberg
Table Of Contents
S. Salzberg, RD, LD, CDE
Clinical Dietitian, Department of Nutrition Services, Northwestern Memorial Hospital, Chicago, Illinois (Vol 2, Chap 7)
“FETAL ORIGINS” HYPOTHESIS
INITIAL PRENATAL VISIT
NURITIONAL REQUIREMENTS OF PREGNANCY
VITAMIN, MINERAL, AND HERBAL SUPPLEMENTS
WEIGHT GAIN RECOMMENDATIONS
COMMON DISCOMFORTS OF PREGNANCY
In 1889, Prochownick performed the first serious study of diet in pregnancy.1 He restricted calories, reduced sodium intake, and encouraged minimal weight gain with the goal of reducing infant size in women with contracted pelves to avoid preterm induction of labor. The size of the babies was successfully decreased; however, even with early induction of labor in women with contracted pelves, infant loss was 50% and approximately 5% of the mothers died.
A woman's nutrition intake before and during pregnancy affects the growth and development of her baby. Increased folic acid intake before and during pregnancy has been shown to help reduce the development of neural tube defects.2,3 Excessive vitamin A intake, especially in early pregnancy, has been shown to be teratogenic to the fetus.4 In 1990, the Institute of Medicine (IOM) did an extensive review of the data on pregnancy and made recommendations for weight gain, dietary intake, and nutrient supplementation. They concluded that pregnant women should gain weight based on their pregravid body mass index (BMI), receive counseling on a healthy diet to meet recommended weight gain, and be monitored regularly to identify potential problems, with early intervention when indicated. The IOM also concluded that all pregnant women should have a routine assessment of dietary intake and recommendations for improved diet or vitamin and mineral supplements throughout pregnancy.5 The obstetrician is usually the first person from whom the pregnant woman seeks nutrition information. Specific recommendations should be based on nutritional needs and individualized for each woman, taking into account cultural and ethnic background and views regarding diet and health. The impact of pregnancy is not always seen immediately, and may not be seen in the pregnant woman but may manifest in the infant.
The perinatal period is an exciting time. There is a growing amount of evidence that maternal nutrition before and during pregnancy can affect the fetus at birth and throughout life.6 Most pregnant women become more interested in their body and in health when pregnancy is confirmed. What they eat becomes more important. They are more concerned about their weight and body image. Most women enter pregnancy with calcium intakes below the Recommended Dietary Allowances (RDA) of 1000 mg/day before pregnancy. When pregnancy is confirmed, women often attempt to increase calcium intake. Many women report that they eat better at the beginning of pregnancy; however, they don't necessarily continue the changes throughout pregnancy, for reasons that are not always apparent.
What a woman eats before pregnancy is as important as intake during pregnancy. For women of childbearing age, every gynecology visit should include a nutrition assessment. The assessment should include BMI status; chronic disease requiring medical nutrition therapy; drug, alcohol, smoking, vitamin, mineral, and herb intake; history of eating habits; and an assessment of disordered eating or other psychosocial issues that may impact nutritional intake. Folic acid supplements should be initiated and iron status should be assessed for all women of childbearing age. Weight loss should be encouraged for overweight women before contemplating pregnancy due to the increased risk of gestational diabetes and hypertension associated with obesity.7 Women who are underweight should be encouraged to gain weight before pregnancy to decrease the risks of small-for-gestational age and low-birth-weight infants. The cause of the low BMI should be evaluated; some common causes are disordered eating behaviors, drug use, excess exercise, or gastrointestinal disorders. Women with a history of a chronic illness requiring intervention with medical nutrition therapy should be evaluated to assure good control of their diet and disease status. Referrals to a registered dietitian should be encouraged for all women before pregnancy is attempted.
|“FETAL ORIGINS” HYPOTHESIS|
The “fetal origins” hypothesis is currently getting much attention. Research is underway to test the hypothesis that nutrition insults during critical stages in fetal growth and development may have profound and long-lasting effects on the subsequent health of the fetus.6,8 It is proposed that during the critical periods of growth, an insult caused by either maternal illness or change in the nutrients supplied to the fetus can interrupt the genetic programming for hormonal axis, causing an increased risk for diseases in adult life.9 A study of a group 15,726 men and women born between 1911 and 1930 in Hertfordshire, England10 showed a reduction in death rates from coronary heart disease as birth weights increased. Similar findings were seen in a study based on 70,000 men and women in the United States,11 and a study of 1200 men in South Wales.12 Birth weight has been inversely related to the development of adult disease such as hypertension, diabetes, and heart disease. In adults with type 2 diabetes, those with the lowest birth weights and who are obese as adults appear to have a decrease in the number of functioning β-cells, which causes a decrease in insulin production in adulthood.13 There is also evidence that the time of the nutrition insult may have different effects on adult disease risk. For example, it is thought that a fetal growth trajectory is established early in pregnancy. If nutrients and calories delivered to the fetus are decreased in early pregnancy, the fetus may adapt to a lower energy requirement. This will prevent increased growth later in pregnancy despite an increase in energy and nutrient intake later. Similar findings were seen in women who drink alcohol during pregnancy. If alcohol intake is stopped by the second trimester, growth is still impaired.14 The timing of the nutrition insult may be important in determining the long-term health of the infant even when birth weight is normal. Other studies have not shown the same relationship to maternal nutrition. Matthews and Yudkin concluded that maternal nutrition in industrialized countries seems to have a small effect on placental weight and birth weights.15 At the Montreal Diet Dispensary, the effects of increasing nutrition and its effects on birth weights have been well established.16 Some suggest that the fetus is not a “perfect parasite” and in fact there is “a complex hormonally orchestrated metabolic interplay between the competing needs of the fetus and the mother.”17 More research is needed to determine the effects of the timing and degree of nutrition insults on the incidence of disease in adult life. In the meantime, woman should be encouraged to eat a balanced diet to meet the weight gain goals and nutritional requirements of pregnancy.
|INITIAL PRENATAL VISIT|
The initial prenatal visit should include a complete assessment of all the components that may impact a woman's nutritional status before and during pregnancy.
Nutrition assessment requires a holistic approach. Eating behaviors are a personal issue, and how or why a person eats is determined by emotional, physical, and cultural beliefs. The four major components of a nutrition assessment are medical, nutrition, psychosocial, and obstetric histories. The medical history is used to determine preexisting conditions that required medical nutrition therapy. If a special diet was required before pregnancy, make an assessment to see if any changes are needed. The past obstetrical history can help to identify nutrition-related problems. A previous low-birth-weight infant or a large-for-gestational age baby can indicate a nutrition problem requiring nutrition intervention. A psychosocial assessment should include information on the patient's feelings about the pregnancy, her support system, emotional status, and body image. Whether the pregnancy was planned or unplanned may determine the motivation a woman has to improve her diet. The woman's support system or lack of support during the pregnancy also affects her eating behavior.
The dietary history should begin with a measured height and weight, pregravid weight, BMI determination (Fig. 1), and weight gain in the current pregnancy. A weight and dieting history can help determine any previous or current eating disorder. Possible signs of an eating disorder include a fear of being weighed or refusing to be weighed, poor weight gain, multiple food aversions, ongoing nausea and vomiting, inappropriate body image, eroded tooth enamel, dehydration, enlarged salivary glands, and low prepregnancy weight. Vitamin, mineral, and herb use should be obtained, and food resources, such as cooking facilities and food availability, should be assessed. The Women, Infants, and Children's Program (WIC), which provides milk, eggs, cheese, cereal, and juice throughout pregnancy and lactation, is available to low-income pregnant women based on medical need. Cultural and religious food practices and beliefs should be assessed because they may impact the nutritional intake of a pregnant woman. For example, fasting is required in some religions, and in pregnancy this would not be encouraged. A diet history can be obtained through several different methods. The diet history can be done by a 24-hour recall, where a person relates what they ate during the previous 24 hours. Other methods are a food frequency questionnaire, which lists foods and the frequency per day or per week, and a 2- to 3-day diet diary, which keeps track of actual intake for the specified time. These methods are often combined to cross check information given. A woman may say she drinks four glasses of milk a day, but further questioning may reveal that she buys only one gallon of milk a week. This would be equivalent to two 8-oz glasses a day, instead of the four reported. It is important to include all foods eaten and beverages consumed. Timing of meals and portions should be ascertained to properly assess the pregnant woman's intake. Questioning a woman about her intended infant feeding practices can begin the process of encouraging breastfeeding.
The first visit should summarize the nutrition recommendations based on the assessment. Recommendations should include information on weight gain, vitamin and mineral supplementation as needed, promotion of breastfeeding, and treatment of current problems associated with pregnancy, such as nausea, vomiting, heartburn, and constipation. Women found to be at nutrition risk (Table 1) should be referred to a registered dietitian for further assessment and treatment.
Review of Past Obstetrical History
Poor reproductive performance
Adolescent (<16 yr old)
Hemoglobin <33 or hematocrit <11 in first or third trimester
Individual weight gain not meeting IOM guidelines
|NURITIONAL REQUIREMENTS OF PREGNANCY|
The calorie cost of pregnancy is said to be approximately 80,000 calories for the course of pregnancy.18 Calorie requirements should be determined for each individual based on prepregnancy weight, diet history, height, activity level, time of gestation, and weight gain goals. The 1989 RDA for calories is an additional 300 calories per day after the first trimester,19 based on the assessed calorie needs before pregnancy. Energy intake is adequate when the rate of maternal weight gain meets the IOM guideline.5 Additional calories should be derived from foods that were deficient in the pregnant woman's diet before pregnancy. For example, most pregnant women do not meet their calcium requirements before pregnancy; however, an additional 2 cups of low-fat milk will increase calorie intake by 250 calories (or approximately the recommended increase) and provide the additional calcium.
Carbohydrates should constitute approximately 50% of the diet for most pregnant women. Carbohydrates are important for energy production, and they spare protein from being used as energy. Whole grains, fruits, vegetables, milk, yogurt, beans, and peas contain carbohydrates. The carbohydrate group provides much of the fiber necessary to help prevent constipation and hemorrhoids. At present, the safety of a high-protein, low-carbohydrate diet is unknown. Ketones are produced with low-carbohydrate diets, which may be contraindicated in pregnancy. Regular carbohydrate intake is recommended according to the Food Guide Pyramid.
Protein is required for the growth of maternal and fetal tissue. The effects of a protein deficiency on the outcome of pregnancy are difficult to assess. Most women who have low protein intakes also have a caloric deficit. The RDA for protein is 60 g/day to meet pregnancy needs,19 and can be met using protein from animal and plant sources. The average protein intake in the United States is approximately 75 to 110 g/day. Quality as well as quantity of protein should be considered when assessing the protein intake of the pregnant women. Adolescents and women with multiple gestations have increased protein requirements.
Fat requirements are unchanged during pregnancy. The American Heart Association guidelines for fat are 30% of total calories per day. The fat intake of a 2000-calorie diet is 60 g/day. Saturated fats should be limited and the majority of fat should be monounsaturated and polyunsaturated. One serving of monounsaturated and polyunsaturated fats includes foods such as 1 teaspoon of olive, peanut, canola, or corn oil, 2 whole walnuts, 6 almonds, and 10 peanuts, 2 teaspoons of peanut butter, one eighth of an avocado, and 10 olives. Some research has shown that the long-chain polyunsaturated fat acids, in particular docosahexaenoic acid (DHA) and arachidonic acid (AA), in the maternal diet play a role in fetal growth and development.20 DHA and AA (n-3 fatty acids, found in fish, shellfish, flaxseed, walnuts, and canola oil) have been associated with neonatal brain development and visual acuity of infants. They may also have a role in improving birth weights, decreasing the incidence of intrauterine growth retardation, and preventing preeclampsia.21 The quantity, ratio of n-3 to n-6 fatty acids, and level of safety have not yet been established. Until then, no specific recommendations can be made for pregnant women.
Vitamin A is required for its role in vision, cellular growth and differentiation, and immune function. Vitamin A deficiency in HIV-positive pregnant women has been shown to increase maternal-fetal transmission in parts of Africa. Further studies are underway to identify the role of vitamin A in this population.22 Vitamin A is readily available in the food supply of the United States. The best food sources of vitamin A include leafy green and orange vegetables, such as spinach, dark green lettuce, carrots, sweet potato, acorn and butternut squash, cantaloupe, and apricots. Vitamin A deficiency is rare in industrialized countries, but quite common in other parts of the world. In rat studies, vitamin A deficiency showed impaired lung development23 similar to that seen in premature babies with respiratory distress syndrome. These babies are often found to be vitamin A deficient. The vitamin A content of breast milk is associated with the vitamin A status of the mother during the third trimester of pregnancy. Breast milk of the mildly undernourished woman can be vitamin A deficient after the first few weeks of lactation, putting the infant at risk for health problems related to inadequate vitamin A.24,25
A greater concern regarding vitamin A is the teratogenic effect in animal and human studies of excess intake of preformed vitamin A (retinol).4,26,27,28 Beta-carotene, a precursor of vitamin A, does not seem to be teratogenic. In humans it has been found that isoretinoin, a vitamin A analog, has been associated with fetal anomalies involving the central nervous system, and craniofacial, cardiovascular, and thymus malformations.29 Due to the possibility of its teratogenic effects, the World Health Organization (WHO) recommends that vitamin A intake in supplements used before or during pregnancy should not exceed 10,000 IU/day (3000 μg).30 The Teratology Society of the United States recommends total vitamin A intake from food or supplements should not exceed 8000 IU/day (2400 μg).31 In 2001, the Food and Nutrition Board of the National Academy of Sciences recommended a Dietary Reference Intake (DRI) of 770 μg (2500 IU) of vitamin A for pregnant women and an upper tolerable limit of 3000 μg (10,000 IU) per day.32 The IOM recommends avoiding vitamin A supplements, especially in the first trimester.5 Preformed vitamin A is found only in animal products, such as meat, milk, eggs, fish, and chicken. Beef liver has more than three times the amount of preformed vitamin A than is currently recommended. Provitamin A beta-carotene sources includes dark green leafy and orange vegetables and fruits. When vitamin A supplements are prescribed, it is important to check the source of the vitamin A. Some prenatal vitamins do not identify the source of vitamin A as either preformed vitamin A or beta-carotene. Avoid vitamins that do not list the specific type of vitamin A. Women with a low serum retinol concentration and poor intake of vitamin A would require supplementation.
Inadequate intake of folic acid periconceptually is associated with an increased risk of neural tube defect. An additional 400 μg of folic acid used 3 months before and for the first 12 weeks of pregnancy has been shown to decrease the occurrence of neural tube defect by 70%.2,3 In addition, the Centers for Disease Control and Prevention recommend that to prevent recurrence of neural tube defect, a folic acid supplement of 4 to 5 mg/day should be consumed.33
Folic acid is necessary as a coenzyme in single-carbon transfers from one compound to another. This is important, especially in pregnancy, in the synthesis of several amino acids involved in nucleic acid synthesis. A deficiency of folic acid in pregnancy may impair cell growth and replication and has been associated with poor pregnancy outcome.34 Three sources of folate are currently available. The first source is folate naturally occurring in food. The bioavailability of dietary folate is approximately 50% of synthetic folate.35 In 1998, the Food and Drug Administration (FDA) required that enriched grains be fortified with folic acid 1.4 μg/g of product.36 These fortified foods are the second source of folic acid. A recent report suggests the incidence of neural tube defects in the United States has decreased by 19% since the introduction of folate-fortified foods.37 The third source of folic acid is synthetic folate from vitamin supplements. Folic acid in fortified foods and those provided by supplements are absorbed at a rate of 85% to 100%.38
The recommended DRI for folic acid in pregnancy set by the Food and Nutrition Board of the National Academy of Sciences is 600 μg/day with an upper tolerable intake level of 1000 μg/day.39 A level of 600 μg/day was found to maintain normal folate status. This level can be achieved with a diet high in naturally occurring folate and a supplement of 400 μg/day. Dietary sources of folate include leafy green vegetables, orange juice, strawberries, dried peas, beans, and foods enriched with folate such as whole-grain breads, pasta, rice, and cereals. Women at risk for folic acid deficiency includes those with low dietary intake, and those who use medications that are folate antagonists such as trimethoprim, triamterene, carbamazepine, phenytoin, phenobarbital, and primidone.
Most pregnancies are unplanned, and even those that are planned often do not meet the recommendation for folate. At their gynecology visits, women of childbearing age should be advised to take a folic acid supplement and include good food sources of folic acid in their diets.
Iron-deficiency anemia is the most common form of nutritional deficiency. The rate of iron-deficiency anemia is high among low-income pregnant women. No improvement in anemia has been seen in this group since the 1970s. Iron-deficiency anemia is associated with a higher incidence of low-birth-weight infants and a shorter length of gestation. Trials have shown that when iron supplementation was provided, the incidence of low-birth-weight infants was decreased.41
Iron absorption is increased during pregnancy and depends on maternal iron stores. Heme iron (iron from animal sources) is two to three times more absorbable than non-heme iron, plant-based foods, and iron-fortified foods. Non-heme iron is better absorbed in the presence of heme iron and vitamin C. Absorption is impaired when consumed with phytate (e.g., bran, whole grains), calcium (especially calcium in supplements), tannin in teas, and polyphenol in some vegetables.
The Continuing Survey of Food Intakes by Individuals (1994 to 1996) (CSFII)42 suggests that one quarter of adolescent girls and women of childbearing age meet the RDA for iron through diet. National Health and Nutrition Examination Survey (NHANES) III data indicate 11% of non-pregnant women 16% to 49% had iron deficiency and 3% to 5% had iron-deficiency anemia.43
The dietary reference intake for iron is 27 mg/day. The tolerable upper level of intake is 45 mg/day.32 In 1998, the Centers for Disease Control and Prevention made recommendations for preventing and treating iron-deficiency anemia during pregnancy. Primary prevention includes recommending iron supplementation (30 mg) for all pregnant women at the first prenatal visit, encouraging dietary iron from foods with high iron content, and increasing foods that enhance iron absorption. Iron supplementation may be beneficial to prevent women from entering a subsequent pregnancy with low iron stores. For secondary prevention, they recommend screening for anemia at the first prenatal visit.44 The guidelines for anemia recommended by the IOM should be followed. The cutoff values for anemia in pregnancy are as follows: first trimester, hemoglobin 11 and hematocrit 33; second trimester, hemoglobin 10.5 and hematocrit 32; and third trimester, hemoglobin 11 and hematocrit 33.5 Treat anemia with iron supplementation, 60 to 120 mg/day, and discuss dietary changes to improve absorption and intake. When hemoglobin and hematocrit become normal, decrease iron to 30 mg/day.44 Studies are being done to determine the best way of dosing iron, and have looked at weekly, daily, and multiple daily dosing. Compliance with iron supplementation is often poor because of associated gastrointestinal side effects.
Calcium is important for bone and tooth formation and maintenance, and is required in nerve transmission and regulation of the heartbeat. During pregnancy, calcium is transferred to the fetus at a rate of approximately 330 mg/day by the third trimester.5 Calcium absorption and urinary excretion of calcium are greater than before pregnancy. These changes are noticeable before fetal calcium demands are actually increased.45 Multiple studies have measured the changes in bone density in pregnant and lactating women. Bone mineral losses are seen by 3 months postpartum, and by 5 months after menses begin the bone mineral content returns to prepregnant status.46,47 Lactating adolescents are the one group at risk for permanent bone loss. One study of lactating adolescents showed bone loss in the forearm of those not supplemented with calcium, whereas those supplemented with calcium had little to no bone loss.48 A study of Indian women with typical calcium-deficient diets showed that neonates whose mothers received a calcium supplement had higher bone density than those whose mothers did not receive a supplement.49
Low calcium intake has also been associated with an increased risk of pregnancy-induced hypertension. In some studies, calcium supplements have been shown to reduce blood pressure of pregnant women and their offspring. Bucher conducted a metanalysis on 14 randomized controlled trials. In most of the studies, the usual calcium intakes were below the RDA for calcium. It was found that 375 to 2000 mg of supplemental calcium had a blood pressure-lowering effect. The study showed calcium supplementation reduced the risk of developing pregnancy-induced hypertension and preeclampsia in women who were normotensive before pregnancy. When a further study was done of women with hypertension, 1000 mg of calcium significantly lowered their diastolic blood pressure.50 Another study done by the Calcium for Preeclampsia Prevention (CPEP) group found no change in blood pressure in a group of women with usual calcium intakes of 1100 mg/day who were given an additional 2000 mg/day by calcium supplement.51 The differences in Bucher's metanalysis and the CPEP study may be explained by the latter group having a normal calcium intake. When calcium intakes are within the normal range, additional calcium may not have a beneficial effect.
The Food and Nutrition Board of the National Academy of Sciences set the Adequate Intake (AI) for calcium in pregnancy at 1000 mg/day for women age 19 to 50 years and 1300 mg/day for adolescents under 19 years. The tolerable upper intake level is 2500 mg/day through diet and nutritional supplement.52 Milk (8 oz), yogurt (8 oz), and cheese (1.5 oz) all provide approximately 300 mg of calcium. Almonds, broccoli, sardines and salmon with bones, soy milk, and calcium-fortified orange juice are also good sources of calcium, although portions vary. Dietary calcium sources should be encouraged. If calcium intake is below the RDA, a calcium supplement should be considered. Calcium carbonate from Tums and other supplements should be taken with a meal. Calcium citrate can be taken with or without meals.
Women enter pregnancy with many different eating habits. Some women eat one meal a day, whereas others consider themselves to be “grazers” who eat many small meals. There is no one way for every woman to meet her nutrition requirements. A study done using the data from the Pregnancy, Infection, and Nutrition Study53 concluded that their study supports animal model work showing an association between decreased frequency of meals and preterm delivery. A 24-hour fast during Yom Kippur also showed an increased rate of spontaneous deliveries.54 The potential for prolonged periods without food can cause hypoglycemia, which may stimulate neuroendocrine events affecting the fetus.55,56 Therefore, meal timing should be considered when assessing and counseling a pregnant woman. Most women find meals are best spaced no more than 5 hours apart. If meals must be more than 5 hours apart, a snack including foods from the Food Guide Pyramid is usually recommended. People who often skip meals or go a long time between meals choose more snacks with low nutrient density or overeat at the meals they do eat. A small bedtime snack (approximately 200 calories) is usually encouraged to avoid a long period overnight without eating and to avoid the possibility of ketosis.
Translating Nutrition Requirements Into Diet Recommendations
After a nutrition assessment, a review of the Food Guide Pyramid (Fig. 2) can guide the woman in her food choices to better meet the requirements of pregnancy. A variety of foods from each of the groups is encouraged.
There is no one perfect food. Foods are used in combinations to provide all of the essential nutrients. Nutrition information provided to each woman should be based on her ethnic and cultural background. Whole-grain breads and cereals are encouraged, with at least 6 to 11 servings per day of a variety of grains. Serving sizes are defined as one-half cup rice, pasta, or cereals, or 1 oz or 1 slice of bread or bread product. Women of various ethnic groups may choose tortillas, naan, chapati, or pita bread as other examples of grains. Grains provide fiber, complex carbohydrates, B vitamins, folic acid, and iron. From the fruit group, 3 to 5 servings are recommended each day. Many pregnant women increase their intake of fruit juices because they decrease diet soft drinks. Fruit juices can add many additional calories without the woman being aware, however. For example, one client of mine consumed more than 1000 calories a day in three servings of fruit juice because her servings were more than the recommended 4 to 6 oz, resulting in a weight gain of 10 lb/month. Although 8 oz of orange juice can provide a good source of vitamin C and folic acid, more than 8 oz may only add additional calories and no fiber. A variety of fresh fruits are encouraged instead of fruit juices. Oranges, strawberries, melons, and other fruits can provide folic acid, vitamin C, and vitamin A in the form of beta-carotene. Vegetables are also recommended, 3 to 5 servings per day, from a variety of fresh or frozen vegetables. Vegetables are good sources of fiber, vitamins A and C, and folic acid, and some are high in non-heme iron. Two medium carrots can provide almost all the vitamin A needed for one day in the form of beta-carotene. Dark green leafy vegetables are good sources of vitamin A and folic acid. Dark green lettuce and tomatoes on sandwiches can provide a serving of vegetables. A serving of vegetables is one cup raw or one-half cup cooked vegetables. Vegetables should be added as a side dish to each lunch or dinner or for snacks. Meat and meat substitutes are recommended, with 2 to 3 servings of 2 to 3 oz each per day. Lean meats, chicken, fish, beans, and peas are recommended. Incorporating beans, peas, nuts, and soy proteins can provide adequate protein intake for pregnant women who follow a vegetarian diet. For lacto-ovo vegetarians, eggs and cheese can be added to meet their protein needs. With proper meal planning, vegetarians are able to meet their protein requirements. Most pregnant women eat approximately 75 to 110 g of protein per day, exceeding their recommended protein requirement for pregnancy. Intake of lunchmeats and high-fat processed meats should be limited. Three or more servings each day are recommended from the milk group, which provides calcium, vitamin D, and protein. A serving includes 8 oz of milk or yogurt or 1.5 oz of low-fat cheese. Chocolate milk, hot chocolate, using milk in soups, adding cheese to sandwiches, or eating yogurt as a snack are ways of increasing calcium intake. Women with lactose intolerance can use lactose-reduced milk. Small, frequent servings of milk products are often better tolerated than larger servings. If calcium intake is less than 1000 mg/day, calcium supplements are recommended.
Women who follow the guidelines in the Food Guide Pyramid should be able to meet the requirements for most nutrients. Iron and folic acid are usually difficult to get from food sources alone. As much of these nutrients should be encouraged from dietary sources as possible and supplements should be recommended.
|VITAMIN, MINERAL, AND HERBAL SUPPLEMENTS|
The IOM recommendations for nutrition supplementation include 400 μ folic acid and 30 mg iron per day for all pregnant women. Risk factors requiring vitamin and mineral supplementation include multiple gestation, drug or alcohol abuser, poor dietary intake with resistance to change, and use of iron supplementation greater than 30 mg/day. A regular prenatal vitamin should be used. The vitamin supplement should include 30 to 60 mg iron, 15 mg zinc, 2 mg copper, 250 mg calcium, 400 IU vitamin D, 50 mg vitamin C, 2 mg vitamin B6, 400 μ folic acid, and 2 μ vitamin B12.5 Care should be taken to check the vitamin A source, and beta-carotene rather than retinol or preformed vitamin A should be used.
All pregnant women should be questioned about use of herbal supplements. Many herbs are contraindicated in pregnancy because of known adverse effects in pregnant women. Dong quai, foxglove, pokeroot, senna, uva ursi, aloe, chaparral, coltsfoot, St. John's wort, black cohosh, comfrey, and pennyroyal are some herbs that are not recommended in pregnancy either because of their potential to induce abortion or cause central nervous system disturbances or diarrhea. Women often hesitate to tell their health care providers about use of herbs because they fear disapproval. Very little data exists on the effects of herbs in pregnancy on the developing fetus. Currently, there is no regulation of herbs in the United States, and what the label says may not be what the bottle contains. Herbal teas bought in the grocery store can be used in moderation (1 to 2 cups/day). Teas bought in health food stores or from herbalists should be avoided because they are not regulated as food or drug items. At this time, it is best to discourage the use of herbs until more data is available.
Caffeine intake has been associated with an increased risk of miscarriage, low-birth-weight infants, and a reduction in birth weights. Most of the studies looked at caffeine intakes as low as 150 mg/day and as high as the equivalent of 7 cups of coffee a day. In 1990, the IOM subcommittee concluded that the data were not sufficient to make any specific recommendations on caffeine intake.5 Nehlig and Derby in 1994 looked at the data from human and animal studies of caffeine intake during pregnancy, and concluded that a moderate consumption of coffee during pregnancy should be advised.57 Moderate caffeine intake is considered to be less than 200 mg/day. Using milk in coffee beverages is a common way for women to increase calcium intake. Mexican women often drink their coffee with at least 4 to 6 oz of milk, which adds more calcium to their diet. Table 2 lists the caffeine content of some beverages and foods.
Alcohol can have direct and indirect effects on the fetus, including a decrease in DNA synthesis, impaired cellular growth and differentiation, changes in placental function, and decrease in glucose and amino acid transfer to the fetus. Spontaneous abortions are twice as likely with moderate alcohol intake (more than 1 oz of alcohol twice a week) and four times more likely with heavy drinking (one to five drinks per day, four times a week). Alcohol is associated with an increase in perinatal mortality, a decrease in birth weights, and an increase in low-birth-weight infants and congenital malformations. Fetal alcohol syndrome is associated with alcohol intake during pregnancy. Binge drinking has the greatest effect on the fetus; however, some reports have shown adverse affects on neonatal outcomes with as little as one alcoholic beverage every day.58,59 Fetal growth was decreased in women who drank throughout pregnancy. Growth was impaired in the infants of women who quit by the second trimester, though not to the same extent as in women who continued to drink.14 This observation may be similar to the “fetal origins” hypothesis. The defects associated with fetal alcohol syndrome may be the result of the amount of alcohol intake at different times of pregnancy having different effects. Until definitive data are available on the level of alcohol intake that is safe in pregnancy, pregnant women should avoid alcohol.
In 1993, the American Dietetic Association prepared a position statement on the use of non-nutritive sweeteners in pregnancy. They stated that saccharin can cross the placenta and limited use was advised. Aspartame was said to be safe in pregnancy except for women with phenylketonuria (PKU). Studies have been done showing that intake of aspartame levels at least three times the 99th percentile have shown no risk to the mother or the developing fetus.60,61 Of the three components of aspartame, aspartate does not cross the placenta. Phenylalanine does cross the placenta, but the amount is unlikely to cause neurotoxicity. Women without PKU have phenylalanine hydroxylase activity to prevent any substantial or sustained rise in serum phenylalanine. Methanol does cross the placenta, but the amount ingested is very small. Acesulfame K is safe for use in pregnancy.62 Sucralose is another non-nutritive sweetener approved for use in 1998. The FDA reported that sucralose was found to be safe for use by pregnant women.63,64
Regular moderate exercise is encouraged during the pregnancy of a healthy woman.65 Pregnant women who exercise should be sure to drink plenty of fluids before, during, and after exercise to prevent dehydration. A small snack containing some carbohydrates should be eaten at least 1 hour before exercise to prevent hypoglycemia. A small snack may also be required after exercise based on the length of time and intensity of the workout. For women with poor weight gain, exercise should be limited or more snacks before and after exercise should be encouraged to meet weight gain goals.
|WEIGHT GAIN RECOMMENDATIONS|
Weight gain recommendations have varied widely over the past 50 years. Weight gain restrictions were common until the 1970s, when the National Academy of Sciences concluded that restricting maternal weight gain was associated with an increased risk of low-birth-weight infants. Weight loss programs during pregnancy were discouraged and weight gain recommendations were liberalized.66 Weight gain and birth weights were increased with the liberalized weight gains.5,67 Quality, quantity, and rate of weight gain are important. A woman can gain 25 pounds from eating chips, colas, and other low caloric-density foods, or with a diet that provides all the essential nutrients.
In 1990, the Institute of Medicine of the National Academy of Sciences again reviewed the literature and published their report confirming the association previously made regarding pregnancy weight gain and birth weights. They redefined weight gain goals for pregnant women. The goals are based on the woman's prepregnancy BMI. Table 3 shows the recommended weight gains based on the BMI and the rate of weight gain recommended by the IOM.5
Many studies have been done over the past 10 years testing the weight gain recommendations made by the IOM. A critical review by Carmichael and coworkers68 looked at the relationship between weight gain and spontaneous preterm delivery. In 11 of the 13 studies, they showed an association between a low rate of pregnancy weight gain and an increased risk of preterm deliveries. The conclusion by the authors was that rate of pregnancy weight gain below the lower limits of the normal weight gain range in late pregnancy, recommended by the IOM, increased the risk for preterm births.
Fetal growth has been associated with maternal weight gain. Low maternal weight gain can cause low-birth-weight infants or babies who are small for gestational age. Excess weight gain can result in large infants (macrosomia or large-for-gestational-age babies). Many studies done over the past 10 years have shown that birth weights increase as maternal weight gain increases, and incidence of low-birth-weight babies decreases with weight gains above the recommended range. Macrosomia does not usually occur until the weight gains exceed the level that is above the recommended range established by the IOM.69 In a well-nourished community in China, weight gain recommendation ranges recently increased. Women who did not reach the lower end of the weight gain ranges had a 2.8 times greater risk of having a low-birth-weight infant.70 Pregnant women and physicians have expressed concern associated with the increased weight gain ranges established by the IOM and postpartum weight retention. The National Maternal and Infant Health Survey examined the association between pregnancy weight gain and weight retention 10 to 18 months postpartum. The women who gained above the IOM guidelines of 16 kg were more likely to have weight gain retention of more than 6 kg. The group of women in or below the normal range for weight gain had retained about the same amount of weight. The National Maternal and Infant Health Survey showed that weight gain retention was less than 1 kg for white women and less than 3 kg for black women gaining weight within the IOM guidelines. Black women are at higher risk for weight gain retention of more than 6 kg at any weight gain. Both black and white women who exceeded the weight gain guidelines of 16 kg were twice as likely to retain more than 9 kg 10 to 24 months postpartum.71 How much of that weight was gained postpartum is unknown.
The rate of weight gain should also be considered when assessing weight gain during the prenatal visit. A Canadian study72 showed that women who gained more weight in the first 20 weeks of pregnancy were more likely to retain more weight postpartum.
Weight gain recommendations continue to be an important factor in pregnancy outcome. Total weight gain and the rate of weight gain should be evaluated for each pregnant woman at each prenatal visit. A registered dietitian should complete a nutrition assessment for those women not meeting the weight gain guidelines recommended by the IOM. Edema should be assessed, especially in women with excess weight gain. Bioelectrical impedence analysis may be a promising tool to better evaluate whether a woman's weight gain is from fat, lean body mass, or fluid accumulation.73
The underweight woman is at increased risk for having a low-birth-weight infant. This risk is increased if she has poor weight gain. A woman with a BMI before pregnancy of less than 19.8 is considered in the underweight range based on the IOM weight gain guidelines. Weight gain recommendations for underweight women are 28 to 40 lb with a rate of gain of approximately 1.2 lb/week.5 These women should have a complete nutrition assessment to assess normal eating habits, previous or current history of an eating disorder, exercise habits, or any metabolic or gastrointestinal disorders that may impact weight status. An assessment should include history of drug use, food availability, and a diet history to determine caloric intake, meal frequency, portions, and adequacy of nutritional intake. Recommendations should be discussed with the patient to improve her nutrition status during the pregnancy and to meet weight gain guidelines.
Maternal obesity increases the risk for perinatal mortality. Women who enter pregnancy with a BMI more than 27 have an increased risk for diabetes, hypertension, thromboembolic disorders, and urinary tract infections.7 Macrosomia is increased, with a greater increase in cesarean section rates. The recommended weight gain for women entering pregnancy with a BMI of 26 to 29 is 15 to 25 lb, with a rate of weight gain of 0.5 to 0.75 lb/week. For women with a BMI more than 29, a weight gain of at least 15 lb is recommended, with a rate of weight gain of 0.5 lb/week. The rate of weight gain should also be considered; less than 0.25 lb/week is not recommended for any pregnant women.5
A diet history should be done to assess usual intake and quality of the diet. The goal of nutrition counseling for this patient is to individualize her diet to meet her calorie and nutrient requirements and maintain weight gain according to the IOM guidelines. Exercise (e.g., walking) should be encouraged. Weight loss diets are not recommended in pregnancy. Referral to a dietitian is encouraged for these women. At least two follow-up visits would be recommended.
A normal-weight woman has a pregravid BMI of 19.8 to 26.0. Her weight gain goals are 25 to 35 lb with a rate of weight gain of 0.5 to 1 lb/week.5 A diet history on the initial visit should assess for inadequate intakes based on the guidelines in the Food Guide Pyramid. Patients should be instructed on adequate weight gain and general requirements of pregnancy for calories, calcium, protein, iron, vitamin A, vitamin C, and folic acid. Weight gain should be monitored each visit to assure weight gain within the normal IOM weight gain range. Any excess weight gain or loss should be evaluated and a referral to a dietitian should be made.
Excess Weight Gain
Excess weight gain can be defined as a weight gain greater than the rate recommended by the IOM guidelines for each BMI group. The IOM recommends a further evaluation of weight gains more than 6.5 lb per month for all pregnant women. If a woman is gaining too much weight, the possible cause should be assessed and recommendations made to improve the weight gain rates. Some questions to consider are listed in Table 4. Pregnant women often believe that they can gain extra weight because no one will notice. They start eating more sweets and foods they felt were “forbidden” before pregnancy. It may help to remind them that excess weight gain needs to be lost eventually, and to encourage regular exercise. In the first trimester, many women find they are more fatigued and exercise routines become less frequent. The decrease in exercise and increase in intake leads to excess weight gain. Women also decrease their use of artificial sweeteners and increase caloric soft drinks and fruit juices, which can easily lead to excess weight gain. Nutritional assessments of many women have revealed that an increased intake of fruit juices is a main contributor to excess weight. Once the possible causes of excess weight gain are assessed, suggestions for change should be discussed with the woman. A dietitian should be consulted to assess the possible causes and recommend the necessary changes to improve weight gain. At least two follow-up visits with the dietitian are indicated to make sure the patient has adhered to the recommendations. After gaining too much weight one month, many women may restrict their intake too much in order to limit weight gain the next month. If a psychosocial issue has been identified, a referral to a social worker or other counselor should be initiated.
Once the causes for excess weight gain are identified, recommendations should be made and discussed with the patient. If needed additional referrals should be made to a registered dietitian and/or social worker or other mental health professional
(Adapted from Institute of Medicine: Nutrition during pregnancy and lactation: An implementation guide. Washington, DC, National Academy Press, 1992)
Poor Weight Gain
Poor weight gain can be defined as weight gain at a lesser rate than that recommended by the IOM guidelines. A woman in the normal BMI range should have a weight gain of 10 lb by 20 weeks gestation, and a woman in the overweight range should have a weight gain of 5 to 7 lb by 20 weeks. Woman with a BMI in the underweight range should have a weight gain of approximately 15 lb by 20 weeks. This may vary depending on the number of pounds she is underweight. The IOM defines poor weight gain as less than 2 lb/month for women with BMI in normal weight range, or less than 1 lb/month for women in the high-to-obese weight range.5 As with excess weight gain, several questions should be asked to assist in evaluating the cause of weight gains below the recommended weight gain ranges for each BMI category (Table 5).
Common causes of poor weight gain are skipped meals, fear of gaining too much weight, an unwanted, unplanned pregnancy, and lack of support by the partner or family members. Often women say they “just aren't hungry” or “the baby isn't hungry.” This is usually a red flag for some other problem and should be evaluated. A referral for nutrition services is recommended to assess the cause of the poor weight gain, discuss a nutrition plan, and make other recommendations. At least 2 or 3 visits are suggested to assure improvements are maintained. Referrals for psychosocial services may be made as needed.
With the increase in infertility treatments, multiple pregnancies are more common. Women with multiples present many nutrition-related problems, including increased needs for calories, protein, vitamins, and minerals. Weight gain recommendations are increased. The IOM guideline for a twin gestation is 35 to 45 lb with a weekly weight gain of approximately 1.5 lb/week. Women with multiples need individualized nutrition counseling to help them meet their pregnancy requirements. Many women are told to increase their fluid intake, which causes early satiety and decreased intake at meals. This often results in poor weight gain. Data have shown that when twin birth weights are similar to that of a singleton birth weight, perinatal mortality declines.5 A study by Luke and colleagues concluded that maternal weight gain and pregravid BMI were predictors of fetal birth weight in twin gestations. They also found that women who were seen by a registered dietitian had the highest weight gains and the lowest incidence of babies weighing less than 1500 g.74
Women pregnant with twins should be encouraged to eat small frequent meals accompanied by small amounts of fluids, and to spread between-meal fluid consumption throughout the day. Calcium intake should be increased, though no exact recommendations have been made for multiples. General nutrition guidelines include eating regular meals, using snacks to add foods missed at regular mealtimes, and adding fluids between meals. If weight gain is poor, fluids with caloric value should be used in place of water. If weight gain is excessive, assess portion sizes, edema, and fluid intake. Make necessary changes in the diet to meet the woman's goals.
Adolescence experience many physical and psychosocial changes. Their nutritional needs are increased at the time of peak growth. Increased growth increases the demand for iron, zinc, folate, calcium, protein, and calories.75 Pregnancy further increases nutrient requirements, as previously discussed. Research indicates that pregnant adolescents may be competing for nutrients with their fetus.76
Due to peer pressure, teens often are more concerned about body image. They may skip meals and eat more foods with low nutrient density; however, intake of fast foods with high fat and saturated fat content often increases. Soft drinks replace milk products, so calcium intakes are below the RDA.
Weight gain recommendations are the same as for pregnant adults, although weight gain at the higher end of the range is encouraged for adolescents. Teens who gained less than 20 lb had babies weighing 400 g less than teens who gained more than 20 lb. The incidence of low-birth-weight babies was 13% for the adolescents gaining less than 20 lb and 1% for those gaining more.77 Pregnant adolescents should be advised to choose foods from the Food Guide Pyramid, and fruits and vegetables should be encouraged. For the adolescent, 1300 mg of calcium are recommended, which would include 4 servings of milk per day. Fast foods and snack foods should be incorporated into their diets to improve adherence. Multivitamins with minerals are recommended on an individual basis.
Pica is the abnormal craving and ingestion of non-food substances with little or no nutritional value. The most common forms of pica are laundry starch and clay or dirt. Pica can also include substances like ashes, ice scraped from the walls of the freezer, kitchen cleansers, mothballs, and many others. Many women in different racial, ethnic, and social groups have reported pica.
Pica can result in poor weight gain due to a reported lack of appetite. This is most often associated with eating ice. The ingestion of clay and laundry starch can cause a decrease in nutrient-dense foods even though weight gain may appear normal or even excessive. A 1-lb box of laundry starch contains approximately 1600 calories. Adverse effects of pica include fecal impaction, constipation, decreased absorption of nutrients (e.g., a decrease of iron absorption when clay is consumed), contraction of fillings in teeth (causing an increase in tooth decay), or hemolytic anemia in the mother or fetus.
It is important to ask questions about pica in a nonjudgmental manner. Examples of nonjudgmental questions that may elicit information: “Is there anything you like to eat now that you didn't eat before you got pregnant?” or “Do you crave anything special?”
Some recommendations for women with pica include replacing laundry starch with nonfat milk powder, eating frozen fruit pops or juices instead of ice, or sucking on hard candies, especially lemon candies or mints. Explaining the possible harmful effects of pica on the fetus and suggesting the alternative behaviors may help.
Mercury Intake From Fish
The FDA suggests that women who are currently pregnant or considering pregnancy should avoid intake of fish containing large amounts of mercury. These include shark, swordfish, king mackerel, or tile fish. The mercury content of these varieties is high enough that it may cause nervous system disorders in the newborn. Up to 12 oz of other fish may be eaten in pregnancy, according to the FDA's Center for Food Safety and Applied Nutrition.78
Pregnant women are at an increased risk for developing listeria, which can cause an increase in miscarriage, fetal death, or severe illness in the mother. Pregnant women are advised to avoid hot dogs or lunch meat unless heated until steaming hot; soft cheeses such as brie, feta, Camembert, blue cheese, and Mexican cheeses like “queso blanco fresco”; fresh pates or meat spreads; smoked fish and seafood like salmon, whitefish, trout, cod, tuna, or mackerel; raw unpasteurized milk or foods containing raw milk.78
|COMMON DISCOMFORTS OF PREGNANCY|
Nausea and Vomiting
Hormonal changes are thought to cause simple nausea and vomiting of pregnancy. Hormonal increases may initiate nausea through the following mechanism:
The gastrointestinal tract is sensitive to the sudden increase in hormones.
Symptoms of nausea may vary. Some women complain of nausea occurring only in the morning. Others experience nausea throughout the day. Many working women find nausea worse in the late afternoon, when they go the longest without eating. Symptoms may be mild or severe.
In simple cases of nausea, symptoms appear around the 6th week of pregnancy and abate by the 12th week. Excessive vomiting can cause weight loss due to an inadequate intake of calories, protein, and minerals. Eating small frequent meals, including a bedtime snack, and drinking fluids between rather than with meals usually improve the nausea and vomiting. Usually, no particular foods can help decrease or increase the nausea. Pregnant women report different food tolerances. When nausea occurs, women commonly eat less frequently in an attempt to avoid vomiting; however, this often seems to exacerbate the vomiting. Timing of meals and snacks and avoiding the feeling of hunger seem to be most important in improving the nausea and vomiting. Some women eat every 2 or 3 hours, whereas others may have to eat more frequently. Most women can go no more than 2.5 hours without eating before the nausea returns. Cooking meals should be avoided if the woman finds that smelling food while cooking increases the nausea. Sandwiches are a good alternative to a cooked meal because of shorter exposure to the food during preparation. It may be recommended to cook when the nausea is decreased, and to reheat the food at mealtimes. Milk in the morning seems to be difficult for many women, but may be no problem later in the day. Women with nausea and vomiting, particularly those losing weight, should be referred to a registered dietitian for individualized counseling. An example of small frequent meals should be reviewed with the patient (Table 6).
Breakfast (within 1 h of waking up)
1 slice toast
2–2.5 h later
1 slice toast or ½ bagel
Lunch (2–2.5 h later)
Half sandwich (meat and cheese)
2–2.5 h later
Dinner (2–2.5 h later)
2 oz meat, chicken
2–2.5 h later
Bedtime snack is very important. All meals can be changed to suit the patient's tastes. Dinner may be a sandwich or other food that doesn't require much preparation. Timing of meals and fluid is very important. Fluids should be consumed 30–60 min after meals.
Hyperemesis gravidarum develops in about 2% of all pregnancies. This is persistent vomiting that often requires hospitalization, intravenous fluids, and electrolyte replacement. Once hydrated, the patient should be encouraged to begin a regular diet with small frequent meals. Most women find the clear liquid diet not easy to tolerate, and do better with solid food. If the vomiting continues, tube feedings or parenteral nutrition may be used.
Progesterone is thought to slow the peristaltic action of the smooth muscles in the bowel. This, combined with the pressure of the enlarging uterus on the bowel, slows motility and causes constipation. Iron supplementation may also contribute to constipation. Increasing fiber intake can minimize constipation. Whole-grain breads and cereals, fresh and dried fruits and vegetables (especially those with skins), and an increased fluid intake can help alleviate constipation. Increased activity is also encouraged.
Heartburn is common in pregnancy, especially in the third trimester. Heartburn results from the pressure of the enlarging uterus on the stomach and intestines. Progesterone decreases the integrity of the cardiac sphincter, allowing a reflux of food and acid. Antacids can be used if needed. Dietary changes can help prevent heartburn. Recommended changes include small frequent meals, fluids between meals, avoiding tight clothing, eating a snack 1 to 1.5 hours before bed time, elevating the head of the bed when sleeping, and avoiding high-fat foods and foods that cause heartburn for the individual woman.
5. Institute of Medicine, Committee on Nutritional Status During Pregnancy and Lactation, Food and Nutrition Board: Nutrition During Pregnancy. Part I, Weight Gain; Part II, Nutrient Supplements. Washington, DC, National Academy Press, 1990
13. Phillips DIW, Hirst S, Clark PMS et al: Fetal growth and insulin secretion in adult life. Diabetologia 37: 592, 1994
26. Hathcock JN, Hattan GD, Jenkin MY et al: Evaluation of vitamin A toxicity. Am J Clin Nutr 52: 183, 1990
27. Werler MM, Lammer EJ, Rosenberg L et al: Maternal vitamin A supplementation in relation to selected birth defects. Teratology 42: 497, 1990
30. World Health Organization: Safe vitamin A dosage during pregnancy and lactation. Recommendations and report from a consultation. Micronutrient series (WHO.NUT/964). Geneva, World Health Organization, 1998
32. Food and Nutrition Board, Institute of Medicine: Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Washington, DC, National Academy Press, 2001. Available at www.nap.edu.
33. Recommendations for the use of folic acid to reduce the number of cases of spina bifida and other neural tube defects. MMWR Morb Mortal Wkly Rep 41:1, 1992. Available at http://www.cdc.gov/epo/mmwr/preview/mmwrthml/ 00019479.htm.
36. Schaller DR, Olson BH: A food industry perspective on folic acid fortification. J Nutr 126 (suppl): 761s, 1996
38. Honein MA, Paulozzi CJ, Matthew TJ et al: Impact on folic acid fortification of the US food supply on the occurrence of neural tube defects. JAMA 285 (23): 2981, 2001
39. Food and Nutrition Board, Institute of Medicine: Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, biotin, and choline. Washington, DC, National Academy Press, 1998. Available at www.nap.edu.
42. US Department of Agriculture, Agricultural Research Service: Data tables: Results from USDA's 1994-96 Continuing Survey of Food Intakes by Individuals and 1994-96 Diet and Health Knowledge Survey (online). Riverdale, MD, US Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, December 1997. Available at http://www.barc.suda.gov/bhnrc/foodsurvey/home.htm.
52. Food and Nutrition Board, Institute of Medicine: Dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride. Washington, DC, National Academy Press, 1997. Available at www.nap.edu.
57. Nehlig A, Debry G: Potential teratogenic and neurodevelopmental consequences of coffee and caffeine exposure: A review of human and animal data. Neurotoxicol Teratol 16: 531, 1994
62. FAO/WHO Expert Committee on Food Additives: Toxicological evaluations of certain food additives and food contaminants. Acesulfame potassium. WHO Food Additive Series No. 18, pp 12–27. Geneva, Switzerland, World Health Organization, 1983
66. National Research Council: Maternal nutrition and the course of pregnancy. Report of the Committee on Maternal Nutrition, Food and Nutrition Board. Washington, DC, National Academy of Sciences, 1970
78. Formanek R: Focuses on the food safety rules issued by the United States Food and Safety Administration Center for Food Safety and Applied Nutrition in January 2001. How to reduce the risks for Listeria monocytogenes bacterium; Health risks of pregnant women and women considering pregnancy regarding fish with mercury; Safety of imported food and eggs. FDA Consumer 35 (2): 15, 2001