A Review of Physiological and Behavioral Changes During Pregnancy and Lactation: Potential Exposure Factors and Data Gaps

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REVIEW A review of physiological and behavioral changes during pregnancy and lactation: Potential exposure factors and data gaps

Jacqueline Moya1, Linda Phillips1, Jessica Sanford2, Maureen Wooton2, Anne Gregg2 and Laurie Schuda1

Exposures to environmental contaminants can pose risks to pregnant women’s health, their developing fetuses, children, and adults later in their lives. Assessing risks to this potentially susceptible population requires a sound understanding of the physiological and behavioral changes that occur during pregnancy and lactation. Many physiological and anatomical changes occur in a woman’s organ systems during the course of pregnancy and lactation. For example, blood volume and cardiac output increase during pregnancy, and other metabolic functions are altered to provide for the demands of the fetus. During lactation, nutritional demands are greater than during pregnancy. There are also changes in behavior during both pregnancy and lactation. For example, water consumption during pregnancy and lactation increases. These behavioral and physiological changes can lead to different environmental exposures than these women might otherwise experience in the absence of pregnancy or lactation. This paper provides a summary of information from the published literature related to behavioral and physiological changes in pregnant and lactating women that may affect their exposure or susceptibility to environmental contaminants, provides potentially useful exposure factor data for this population of women, and highlights data gaps.

Journal of Exposure Science and Environmental Epidemiology (2014) 24, 449–458; doi:10.1038/jes.2013.92; published online 15 January 2014 Keywords: dietary exposure; inhalation exposure; personal exposure

INTRODUCTION During pregnancy and lactation, the female body undergoes a In women, reproductive age begins at the onset of menses and wide array of physical and emotional changes in order to nurture a continues until menopause when menses ends and pregnancy is baby in the womb and to produce milk to breastfeed a baby after no longer possible. Although reproductive age range can vary, it birth. These changes can often alter a woman’s body systems and is often defined as the age range from 15 to 44 years.1,2 In the behaviors so that they perform and act differently than in women United States, there are B60 million women of reproductive age. in the general population. The altered physical condition and Roughly 10% of US women between 15 and 44 years of age changes in behavioral patterns set pregnant and lactating women become pregnant annually. In 2008, there were almost 6.6 million apart as a unique population that may potentially be differentially pregnancies (105.5 pregnancies per 1000 women aged 15–44 exposed to environmental agents. For example, hormonal years) in the United States, of which 4.2 million resulted in live changes occurring during pregnancy affect the woman’s appetite 7 births.1 As shown in Table 1, pregnancy rates vary by age and race. and food intake. In the absence of nausea and morning sickness, 7 The lactation period follows childbirth and is the timeframe pregnant women may increase their food intake. Pica behavior during which milk formation allows for the feeding of (i.e., consumption of non-food or non-nutritive items) can also be 7 the child(ren). The American Academy of Pediatrics re-affirms their more prevalent during pregnancy. In addition, some of the recommendation of exclusive breastfeeding for approximately the physiological changes occurring during pregnancy and lactation first 6 months of life and supports the continuation of breastfeeding may alter the internal dose and toxic response, resulting in health for the first year and beyond if desired by the mother and child.3,4. risks that are different from those of the general population. For Among new mothers, breastfeeding rates increased from 74.6% in example, the increased blood plasma volume and protein binding the early postpartum timeframe in 2008 to 76.9% in 2009. At 6 and changes during pregnancy can alter the volume distribution of 12 months postpartum, 47.2% and 25.5%, respectively, continued to chemicals in the pregnant woman’s body.8 Maternal exposures are breastfeed.5 Breastfeeding rates vary with the mother’s age and also important because they can affect the developing fetus, as other sociodemographic factors. Breastfeeding data stratified by some chemicals can cross the human placenta and be transmitted sociodemographic characteristics for 2008 or 2009 have not been to the infant or child via breast milk. released by CDC. Table 2 provides statistics from 2007 on the A targeted search was conducted of the recent literature percentage of mothers that breastfed and the duration of through 2012 to identify articles and books pertaining to breastfeeding, by the age and race of the mother. The highest physiological and behavioral factors, and related exposure factors percentages of breastfeeding are shown for mothers who are Z30 in any or all of the three trimesters of pregnancy and lactation. The years old and for non-Hispanic white mothers.6 search also generated several studies that present information on

1US Environmental Protection Agency, Ofﬁce of Research and Development, National Center for Environmental Assessment, Mailcode 8623P, 1200 Pennsylvania Avenue Northwest, Washington, DC 20460, USA and 2Battelle Memorial Institute, 505 King Avenue, Columbus, Ohio 43201, USA. Correspondence: Jacqueline Moya, US Environmental Protection Agency, Ofﬁce of Research and Development, National Center for Environmental Assessment, Mailcode 8623P, 1200 Pennsylvania Avenue Northwest, Washington, DC 20460, USA. Tel.: þ 1 703 347 8539. Fax: þ 1 703 347 8694. E-mail: [email protected] Received 22 March 2013; revised 28 October 2013; accepted 2 November 2013; published online 15 January 2014 Changes during pregnancy and lactation Moya et al 450 Table 1. Pregnancy rates for 2008, by age and race (per 1000 women). Population group All ages Age (years) Pregnancy outcome Under 15 15–19 20–24 25–29 30–34 35–39 40–44

All Races All pregnancies 105.5 1.4 69.8 163.0 167.9 141.2 78.5 18.8 Live births 68.1 0.6 40.2 101.8 115.0 99.4 46.8 10.6

White non-Hispanic All pregnancies 87.5 0.5 44.8 124.2 149.8 132.5 71.0 16.2 Live births 60.5 0.2 26.7 82.8 109.7 100.8 45.2 9.6

Black non-Hispanic All pregnancies 144.3 3.8 121.6 261.6 216.2 157.7 81.1 21.3 Live births 70.8 1.4 60.4 131.5 108.8 75.3 36.3 9.3

Hispanic All pregnancies 136.9 2.2 111.5 229.5 197.1 149.2 87.2 23.9 Live births 92.7 1.1 70.3 154.1 142.3 105.3 54.0 14.0 Source: Ventura et al.1

Table 2. Breastfeeding rates for 2007 by maternal age and race Table 3. Examples of physiological changes during pregnancy. (percent of women). Organ system Changes Breastfeeding Breastfeeding Breastfeeding ever at 6 months at 12 months Cardiovascular and Increased cardiac output postpartum postpartum circulatory Increased blood volume, plasma volume, red cell mass, white cell count, and platelet Age (years) production ± ± ± o20 59.7 7.9 22.2 7.5 10.7 5.7 Increased coagulation factors and plasma 20–29 69.7±2.1 33.4±2.1 16.1±1.7 Z30 79.3±1.4 50.5±1.7 27.1±1.6 lipid content Urinary Increased kidney size and weight Race Frequent urination caused by increased Non-Hispanic 76.2±1.4 44.7±1.5 23.3±1.3 blood flow to the kidneys and increased White pressure on the bladder Non-Hispanic Black 58.1±3.1 27.5±2.7 12.5±1.9 Respiratory Increased tidal volume, minute ventilation, Hispanic 80.6±2.4 46.0±3.1 24.7±2.8 respiratory frequency, inspiratory drive, Source: CDC.6 inspiratory capacity, respiratory resistance, and occlusion pressure Decreased respiratory tract conductance, pharmacokinetics in pregnancy from a clinical perspective.8–11 peak expiratory flow rates, and expiratory Although some of the physiological differences between pregnant reserve volume Musculoskeletal Increased bone turnover and bone loss and lactating women and the general population of women may Digestive Slower peristalsis influence absorption, distribution, metabolism, and elimination of Increased appetite and dietary needs chemicals in the body, and may affect maternal or fetal health, Endocrine and Elevated levels of estrogen and progesterone these are not the focus of this review. Instead, this study explores metabolic Production of human chorionic some of the potential exposure-relevant physiological and gonadotropin, prolactin, etc behavioral changes that occur in pregnant and lactating Increased energy expenditure women, and provides available data on exposure factors that Increase in maternal fat stores may be useful for conducting exposure and risk assessments for Source: Gabbe et al.7 these women. Data gaps for evaluating exposure among pregnant and lactating women are also discussed. the hormone leptin has been found to regulate food intake, energy expenditure, and body mass accumulations.12 Repro- PHYSIOLOGICAL AND BEHAVIORAL CHANGES DURING ductive hormones have been shown to affect cardiovascular PREGNANCY AND LACTATION responses to stress,13 and alter lipid concentrations in women.7 During pregnancy and lactation, a number of changes occur Maternal blood volume, plasma volume, red cell mass, white throughout a woman’s body, primarily to support the fetus during cell count, and platelet production are all increased during different stages of development. Some of these changes may pregnancy. The increase in blood volume begins at about 6–8 directly affect the manner and extent to which a woman may be weeks gestation and then continues to increase until reaching a exposed to environmental agents, whereas other changes may plateau at 30–34 weeks, with an overall typical blood volume impact the distribution and metabolism of the agent once it enters increase of 40–50% (although individual increases may range from the body (i.e., internal dose). Table 3 provides some examples of 20 to 100%).7,14 Cardiac output (CO), which is a product of stroke physiological changes by organ systems. This section provides a volume (SV) and heart rate (HR) (i.e., CO ¼ SV Â HR), increases brief overview of some of the physiological and behavioral changes significantly during pregnancy, with the uterus, placenta, and that could potentially affect exposure, internal dose, or body burden. breasts being the main target for most of the increase in CO.7 Data Many of the changes that occur during pregnancy and lactation show that the mean±SD (coefficient of variation) CO in l/h are directed by the body’s reproductive hormones. For example, increases from the pre-pregnancy value of 301±65 (22%) to

Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 & 2014 Nature America, Inc. Changes during pregnancy and lactation Moya et al 451 354±76 (22%), 386±75 (20%), 400±79 (20%), and 391±79 expenditure and sleeping metabolic rate were higher in (20%) at 10, 20, 36, and 38 weeks of gestation, respectively.11 lactating than in non-lactating women. Greater increases in blood and plasma volume and CO are Maternal fat stores increase to a peak in the late second trimester observed in twin and other multiple pregnancies.15 and then decline towards the end of gestation as a result of Total body water increases gradually during pregnancy. mobilization to support the rapidly growing fetus.15,32 The Abduljalil et al.11 conducted a meta-analysis of available total mean±SD (coefficient of variation) total fat mass in kilograms body water data. The analysis shows that the mean±SD increases from a pre-pregnancy mass of 17.14±6.6 (39%) to (coefficient of variation) of total body water in liters increases 19.07±6.7 (35%), 19.80±7.5 (38%), and 22.6±7.0 (31%) at from 31.67±4.6 (15%) before pregnancy to 35.22±1.65 (5%), gestational weeks 13, 27, and 37, respectively.11 Blood plasma 40.14±7.55 (19%), and 46.0±5.5 (13%) at 12, 25, and 40 weeks of levels of lipids (fats/triglycerides, fatty acids, and cholesterol) gestation, respectively.11 Approximately 3.5 l of the total body and lipoproteins also increase in pregnancy,7 but by 8 weeks water is accounted for by the water content of the fetus, placenta, postpartum triglyceride levels return to pre-pregnancy levels and amniotic fluid at term.7 The expansions of the maternal blood (including during lactation).7 During pregnancy, the combined volume by 1500–1600 ml, plasma volume by 1200–1300 ml, and effect of endocrine, metabolic, mechanical, and blood flow red blood cells by 300–400 ml account for additional water.16 The alterations in the body cause a woman’s skin to undergo remainder is attributed to extravascular fluid, intracellular fluid in substantial changes. Most of the changes are cosmetic in nature the uterus and breasts, and expanded adipose tissue.7,11 and are therefore not harmful or associated with risks to the mother During pregnancy, several changes occur in the renal system. or developing fetus.7 However, the blood flow changes during The kidneys enlarge in size and weight increases due to increased pregnancy can alter the absorption of drugs through the skin.15 renal vasculature, interstitial volume, and urinary dead space.7 Behavioral changes can also occur during pregnancy and Changes are also observed as the maternal anatomy changes to lactation. These behavioral changes can include: adaptations, accommodate the growing fetus. This includes decreases in the depression, stress and anxiety, fatigue and sleep deprivation, and capacity of the bladder and increases in the frequency of urinary irritability, and can affect activity patterns and energy expenditure, incontinence. Renal blood flow increases 50–80% in the first dietary and non-dietary intake, and body weight. For example, a trimester, then decreases by full term.15 The increase in renal blood pregnant woman may adapt her behavior to stop smoking, reduce flow results in increased glomerular filtration rates in the range of caffeine, or eat healthier foods to benefit the health of the baby. 40–60%.15 Creatinine clearance also increases by 30–50%.15 They can also alter their time–activity patterns or adapt their Both anatomical and physiological changes occur in the behavior to satisfy cravings for dietary and non-dietary substances. maternal respiratory system during pregnancy to ensure Depression can manifest itself in a host of symptoms and adequate supply of oxygen to the developing fetus.15 These behavioral changes that can include appetite disturbance or include: increase in tidal volume (30–40%), increase in inspira- significant weight change, changes in activity levels, psychomotor tory capacity (5–10%), increase in minute ventilation (30–50%), agitation/retardation, and other symptoms. These symptoms cover decrease in functional residual capacity (20%), decrease in expira- a wide range of behaviors, and depression can therefore look tory reserve volume (20–30%), decrease in residual volume (20%), vastly different from person to person.7,33 Anxiety is cited as one of and a slight decrease in total lung capacity (5%), all of which may many factors that may potentially influence maternal weight gain, potentially affect airborne exposures.7,15,17–19 particularly the low prenatal weight gain among adult women with The increase in progesterone levels during pregnancy results low and normal body mass indexes.34 Fatigue and sleep loss in a decrease in intestinal tone and motility.15 The decrease during pregnancy and lactation are often not intentional, but in intestinal motility leads to an increase in the absorption of rather a result of physiological changes and discomfort of nutrients such as calcium and iron, as well as other substances.15 pregnancy and the demands of a newborn child. Irritability can Calcium metabolism during pregnancy and lactation is a highly have similar effects on diet and body weight, and time use. studied area. Maternal calcium metabolism is adjusted during pregnancy and lactation to enhance the transport of this mineral to the fetus without a long-term alteration in the mother’s EXPOSURE FACTORS FOR PREGNANT/LACTATING WOMEN 15 bones. Pregnant women can be at risk years after lead exposure Exposure factors are factors related to human behavior and due to mobilization of lead from the bone when calcium needs 20 characteristics that help determine an individual’s exposure to an increase in pregnancy. Two studies found limited evidence agent.35 Examples of these include, water and food intake, non- supporting the hypothesis of lead mobilization from the bone 21,22 dietary (e.g., pica) ingestion rates, inhalation rates, time spent at during lactation, , whereas others found that breastfeeding various microenvironments and activities, use of consumer practices and maternal bone lead were good predictors of blood 23 products, and body weight. Because of the physiological and lead levels. Bone turnover is higher during the postpartum behavioral changes that occur during pregnancy and lactation, period. Therefore, the blood lead concentration is shown to be 24,25 exposure factors for pregnant and lactating women may be highest 3–6 months after parturition. This potential risk of lead different than those of the general population of women, and they exposure to the woman and the breastfeeding infant is associated may, in turn, impact the fetus or newborn. The following sections with very low (one half to two thirds the daily recommended 25,26 summarize the available exposure factor data for this population requirements) calcium intakes. It has also been shown that of women. foods high in calcium may have a protective effect against the accumulation of lead in bone.27 Dietary energy requirements increase during pregnancy, on Water Intake average, by an additional 200 kcal/day. Energy expenditure and In order to support the increased total body water content during preferential use of carbohydrates is increased to support fetal pregnancy and lactation, pregnant and lactating women tend to growth and milk synthesis.28–31 Butte et al.30 conducted a study of increase the consumption of water. Results from a national dietary energy expenditures in 76 women (40 lactating and 36 non- survey that included assessment of water intake found that, in lactating) at 37 weeks gestation, and 3 and 6 months postpartum. general, lactating women ingest more water than pregnant Total energy expenditure and its components (basal metabolic women and pregnant women ingest more water than control rate, sleeping metabolic rate, and minimal sleeping metabolic women.36,37 Resulting calculations of 3-day averages found total rate) were observed to be 15–26% higher during pregnancy than water intakes (mean±SD) were 1940±686 ml/day (median 1835) postpartum.30 During the postpartum period, total energy for control women, 2076±743 ml/day (median 1928) for pregnant

& 2014 Nature America, Inc. Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 Changes during pregnancy and lactation Moya et al 452 Table 4. Water ingestion rates of pregnant, lactating, non-pregnant non-lactating, and all women aged 15–44 years, communitya and (total water).

Per capitab

Group Mean 95th percentile

ml/day ml/kg/day ml/day ml/kg/day

Pregnant women 819c (1318c)13c (21c) 2503c (2674c)43c (44c) Lactating women 1379c (1806c)21c (21c) 3434c (3767c)55c (55c) Non-pregnant and non-lactating women, 916 (1243) 14 (19) 2575 (2937) 38 (46) age 15–44 years All women, age 15–44 years 922 (1256) 14 (19) 2605 (2949) 39 (46)

Group Consumers onlyd

Mean 95th percentile

ml/day ml/kg/day ml/day ml/kg/day

Pregnant women 872c (1318c)14c (21c) 2589c (2674c)43c (44c) Lactating women 1665c (1806c)26c (28c) 3588c (3767c)55c (57c) Non-pregnant and non-lactating women, 976 (1252) 15 (19) 2614 (2941) 38 (46) age 15–44 years All women, age 15–44 years 985 (1265) 15 (20) 2732 (2953) 39 (46)

Abbreviations: CSFII, Continuing Survey of Food Intakes by Individuals; NHANES, National Health and Nutrition Examination Survey. Source: Kahn and Stralka.2 aIngestion rates for combined direct and indirect water from community water supply. bPer capita intake rates are generated by averaging consumer-only intakes over the entire population (including those individuals that reported no intake). cEstimates are less statistically reliable based on guidance published in the Joint Policy on Variance Estimation and Statistical Reporting Standards on NHANES III and CSFII reports: NHIS/NCHS Analytical Working Group Recommendations.76 dConsumer-only intake represents the quantity of water consumed only by individuals that reported consuming water during the survey period.

women, and 2242±658 ml/day (median 2164) for lactating As shown in Table 4, mean total water intake in units of ml/day was women. As exposure to potential toxic substances in the water highest among lactating women and lowest among non-pregnant supply may be a concern, tap water intake was also calculated and non-lactating women. For community water only, mean intake and found to be 1157±635 ml/day (median 1065) for control in units of ml/day was highest among lactating women and lowest women, 1189±699 ml/day (median 1063) for pregnant women, among pregnant women. and 1310±591 ml/day (median 1330) for lactating women.37 However, it has been noted that because the consumption of bottled water has increased in the United States since the 1977– Dietary Intake 1978 survey on which the calculated water consumption rates Appetite increases during pregnancy to support the needs of the were based, the results are likely to overstate current consumption developing fetus. More calories, protein, and other nutrients are patterns for home tap water.36 required for the growth of the baby, placenta, and uterus.38 USDA Kahn and Stralka2 used data from the 1994–1996 and 1998 recommends no increase of caloric intake during the first trimester, Continuing Survey of Food Intakes by Individuals to estimate an increase of 340 kcal/day during the second trimester, and drinking water intake among pregnant women, lactating women, 450 kcal/day during the third trimester.39 Table 5 shows pregnant non-pregnant and non-lactating women between 15 and 44 years women’s recommended number of daily servings for each of the of age, and all women of 15–44 years of age. A total of 70 pregnant food groups in the food pyramid for three calorie levels (i.e., women, 41 lactating women, and 2221 non-pregnant and non- 1600 kcal, 2200 kcal, and 2800 kcal).40 In addition, energy needs lactating women of 15–44 years of age were identified as meeting during lactation increase by 500 kcal/day compared with non- these criteria in the data set. Kahn and Stralka2 reported consumer- lactating women. Prolactin, the hormone responsible for milk only and per capita water ingestion estimates for both community production, is believed to stimulate appetite and food intake.41 water only and all sources of water. Community water was defined Research of dietary intake among pregnant women in the as tap water from a community or municipal water supply. All United States has been limited to studies regarding nutrient intake sources included tap water from the community water supply as during pregnancy (e.g., calcium and folic acid), changes in eating well as bottled water, water obtained from wells, springs, and patterns due to pregnancy, or associations between pregnancy cisterns, and other sources that could not be identified. The intake outcomes and a specific contaminant intake (e.g., mercury in estimates included direct water ingestion (i.e., as a beverage) and fish).42–45 Crozier et al.46 conducted a study in Southampton, UK, indirect water ingestion (i.e., water added to foods and beverages to assess the consumption of 48 foods or food groups among a during final preparation), but commercial water added by a group of 12,572 non-pregnant women, 2270 women in early manufacturer (i.e., water contained in soda or beer) and intrinsic pregnancy, and 2649 in late pregnancy. Using a food frequency water in foods and liquids (i.e., milk and natural undiluted juice) questionnaire, Crozier et al.46 found that intake of some foods or were not included. Table 4 provides the mean and upper percentile food groups increased in early and late pregnancy, whereas data for four groups of women: pregnant, lactating, non-pregnant consumption of other foods decreased during pregnancy. and non-lactating women 15–44 years old, and all women 15–44 Although these consumption patterns or food choices may not years old. The data are presented in units of ml/day and ml/kg/day. be representative of pregnant women in the United States, they

Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 & 2014 Nature America, Inc. Changes during pregnancy and lactation Moya et al 453 consumed by 154 White women who represented a control group. Table 5. Pregnant women recommended number of servings for Locally caught fish intake was estimated using information on three calorie intake levels. food frequency and dietary history collected via interviews. Calorie level (kcal/day) Table 6 provides information on the number of fish meals consumed by the two groups of women during each of three time periods (i.e., 41 year before pregnancy, r1 year before 1600 2200 2800 pregnancy, and during pregnancy) for the whole population Bread (grain group) 6 9 11 surveyed and for consumers only. The mean number of local fish Vegetable group 3 4 5 meals consumed per year by Mohawk respondents declined over Fruit group 2 3 4 time, from 23.4 (41 year before pregnancy) to 9.2 (o1 year Milk group 3 3 3 before pregnancy), to 3.9 (during pregnancy); there was also a Meat group (ounces) 5 6 7 decreasing trend over time in consumption among controls, although it was much less pronounced. Source: USDA (Department of Agriculture).40 Studies that focus specifically on fish consumption rates for lactating women could not be located. Most studies for this population relate to contaminants found in fish, human milk and their possible association with fish consumption, risk benefit Table 6. Mean number of local fish meals consumed per year by time analyses, or health outcomes. period.

Mohawk women Control group Non-Dietary Intake (Pica) All respondents The term ‘‘pica’’ generally refers to behavior associated with the 41 Year before pregnancy 23.4 10.9 intentional ingestion of foreign (i.e., non-food or non-nutritive) r1 Year before pregnancy 9.2 10.7 substances.49 The types of materials ingested can include: dirt, During pregnancy 3.9 7.3 clay, cigarette ashes, ice, freezer frost, flour, baking soda or powder, cornstarch, powdered milk, or other materials.50 Soil pica Consumers only has been used to refer to the recurrent ingestion of large 41 Year before pregnancy 27.6 23.0 quantities of soil.51 ‘‘Geophagy’’ refers to a specific type of pica in r1 Year before pregnancy 10.9 23.0 51 During pregnancy 4.6 15.5 which earth (i.e., soil or clay) is ingested. Studies have indicated that pica behavior may be more prevalent among pregnant Source: Fitzgerald et al.48 women than among non-pregnant women, and some researchers have theorized that this behavior may result from the desire to satisfy cravings or hunger due to poor nutrition, the need to show that there may be differences in food intake rates and supplement minerals (e.g., calcium or iron) in the diet, cultural preferences between pregnant and non-pregnant women, and practices, or other physiological needs49,52–54 Other researchers that they may change during each trimester. believe that geophagy among pregnant women is best explained Fish consumption during pregnancy and lactation is particularly as protection against symptoms of gastrointestinal distress and of interest to health officials because, although fish is a healthy the effects of harmful chemicals, parasites, and pathogens.55,56 choice and a good source for omega-3 fatty acids and other They proposed that the alleviation of nutrient deficiency is nutrients essential for fetal neurodevelopment, fish may also somewhat unlikely, as geophagy occurs nearly twice as frequently contain contaminants that are harmful to the developing fetus in early pregnancy than in late pregnancy when nutrient and nursing infant. Xue et al.45 conducted a study of 1024 requirements are the highest. pregnant mothers in five Michigan communities. The mean total There was only one study in the literature that observed fish consumption among these pregnant mothers during the first pica behavior for the general population and the population 6 months of pregnancy was 19.6 meals/6 months (3.3 meals/ of pregnant women at the national level. Gavrelis et al.57 month). Oken et al.47 reported a decline in fish consumption conducted an analysis of data from the National Health and among pregnant women following the US Food and Drug Nutrition Examination Survey (NHANES) for the years 1971–1975 Administration’s 2001 national mercury advisory. Food frequency (NHANES I) and 1976–1980 (NHANES II). Gavrelis et al.57 found that questionnaires were completed by 2235 pregnant women in the prevalence of ingestion of non-food substances among eastern Massachusetts. The mean number of meals of fish pregnant females 12 years and older was more than twice that consumed was 7.7 meals/month and 6.4 meals/month before of non-pregnant women in both NHANES I and NHANES II. and after the mercury advisory, respectively.47 Although Gavrelis et al.57 did not report on the prevalence of pica Another study of 22 pregnant women in the Boston area was behavior based on NHANES II data, the pica prevalence based on conducted to assess women’s knowledge of the health effects of NHANES I survey was 2.5% (CI ¼ 0.0–5.6%) for pregnant females 12 fish consumption during pregnancy and determine any changes years and older compared with 1.0% (CI ¼ 0.7–1.4%) for non- in consumption once becoming pregnant.43 Eleven women pregnant females. reported eliminating consumption of sushi during pregnancy.43 Other studies investigated pica behavior among pregnant Others eliminated or reduced certain fish species from their diets women in specific areas of the United States. Bronstein and during pregnancy.43 This reflects behavioral changes (i.e., Dollar49 conducted a study among mostly low-income pregnant adaptation) among these women. Studies comparing fish Black women in urban and rural areas of Georgia. A total of 16% of consumption on a national scale before and after pregnancy the 410 women in the study reported pica behavior, with laundry were not located in the literature. starch and chalk being the most common substances ingested. Limited information is available on fish intake among pregnant Table 7 shows the frequencies of pica behavior and the types of native American women. Fitzgerald et al.48 compared the fish substances ingested. Vermeer and Frate58 conducted a similar consumption habits of 97 nursing Mohawk women 41 year survey among pregnant Black females in rural Mississippi. Of the before pregnancy, r1 year before pregnancy, and during 142 women included in the study, 40 (28%) reported that they pregnancy. The number of local fish meals consumed by these engaged in geophagy (regular consumption of clay) and 27 (19%) women was also compared with the number of local fish meals reported other types of pica behavior, including the consumption

& 2014 Nature America, Inc. Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 Changes during pregnancy and lactation Moya et al 454 Table 7. Frequency of pica behavior. Table 9. Inhalation rates of pre-pregnant, pregnant, and postpartum lactating women, ages 11–55 years.a Rural Urban Total Group Mean 95th percentile N % N % N % m3/day m3/kg/day m3/day m3/kg/day Non-pica 172 82 172 86 345 84 Pica 37 18 28 14 65 16 11 to o23 years Total 209 100 201 100 410 100 Pre-pregnancy 14.55 0.252 18.71 0.339 Chalk 16 42 8 27 24 35 Pregnant, 9th week 19.99 0.344 25.89 0.468 Pregnant, 22nd week 22.59 0.360 30.75 0.500 Starch 14 37 17 57 31 46 Pregnant, 36th week 23.27 0.329 31.07 0.453 Clay 3 8 3 10 6 9 Postpartum, lactating, 23.28 0.342 28.98 0.499 Other 5 13 2 7 7 10 6th week Postpartum, lactating, 23.08 0.352 28.73 0.527 N, number of women exhibiting the behavior. 27th week Source: Bronstein and Dollar.49 23 to o50 years Pre-pregnancy 13.66 0.222 17.87 0.285 Pregnant, 9th week 19.00 0.308 24.49 0.395 Table 8. Items ingested by low-income Mexican-born women who Pregnant, 22nd week 21.36 0.321 28.43 0.433 practiced pica during pregnancy in the United States (N ¼ 46). Pregnant, 36th week 22.14 0.297 29.27 0.399 Postpartum, lactating, 22.15 0.309 27.53 0.425 6th week Item ingested Number (%) Postpartum, lactating, 21.96 0.317 27.29 0.441 ingesting items 27th week

Dirt 11 (24) 50 to o55 years Bean stonesa 17 (37) Pre-pregnancy 13.79 0.229 17.02 0.287 Magnesium carbonate 8 (17) Pregnant, 9th week 19.02 0.314 23.38 0.400 Ashes 5 (11) Pregnant, 22nd week 21.53 0.330 28.30 0.439 Clay 4 (9) Pregnant, 36th week 22.20 0.303 28.53 0.401 Postpartum, lactating, 22.31 0.316 26.70 0.434 Ice 18 (39) b 6th week Other 17 (37) Postpartum, lactating, 22.12 0.325 26.47 0.453 27th week Abbreviations: N, number of individuals reporting pica behavior. 53 Source: Simpson et al. Source: Brochu et al.61 a Little clods of dirt found among unwashed beans. aData for normal-weight women. Number of simulated women ¼ 5000. bIncluding eggshells, starch, paper, lipstick, pieces of clay pot, and adobe.

drive a state of chronic hyperventilation, which has been observed 7,15 of laundry starch, dry powdered milk, and baking soda. Among a to increase tidal volume by up to 30–40% at 8 weeks gestation. sample of 125 pregnant women from a rural area of Georgia, The increases in tidal volume result in an overall rise in minute Smulian et al.54 found the overall pica prevalence to be 14.4%; the ventilation rate by up to 30–50%. As the minute volume increases, rate was 17.8% among Black women, 10.6% among White women, oxygen uptake and consumption also increases. Oxygen consump- and 0% among Hispanic and Asian women. The most common tion has been observed to be 20–40% greater in pregnant women substances consumed were ice, clay, laundry starch, and soap. Of than in non-pregnant women due to the oxygen requirements of 14 the women that reported geophagy, the amounts consumed were the fetus, the placenta, and maternal organs. 61 estimated to range from 0.5 to 1 pound per week.54 Brochu et al. estimated the physiological daily inhalation rates Simpson et al.53 found that 31% of a sample of 225 Mexican- for pregnant and lactating females between 11 and 55 years of born women living in California, who were pregnant or had been age using data on total daily energy expenditures and energy pregnant the previous year, reported pica behavior. The women costs for growth, pregnancy, and lactation. Inhalation rates were reportedly engaged in the behavior because of the taste, smell, or estimated for underweight, normal-weight, and overweight/ texture of the items, for medicinal purposes, because of advice obese females at pre-pregnancy, at weeks 9, 22, and 36 during from someone, or for religious reasons. Speciﬁc quantities of the pregnancy, and for lactating women at weeks 6 and 27 post- pica substances ingested were not provided in the study, but partum. Table 9 provides the mean and 95th percentile inhalation 61 61 Table 8 provides information on the percentage of women rates reported by Brochu et al. Brochu et al. estimated reporting ingestion of various types of items. Klitzman et al.59 inhalation rates to be higher in normal-weight subjects interviewed 33 pregnant women in New York City, whose blood throughout pregnancy and during lactation (through at least 27 lead levels were 420 mg/dl. One of the sources of lead exposure weeks postpartum) than before pregnancy. among individuals in the general population has been the ingestion of non-food items.60 Thirteen of the women (39%) reported pica behavior during their current pregnancies, 10 Activity Factors and Consumer Product Use reported eating soil, dirt, or clay, 2 reported pulverizing and eating Information on activity factors and consumer products use for pottery, and 1 reported eating soap. Quantitative information was pregnant and lactating women is extremely limited. Although not provided for most of the women, but one woman reported several studies have been conducted to analyze relationships eating approximately one quart of dirt daily from her backyard between on physical activity (e.g., exercise) and birth weight or over a 3-month period. pregnancy outcome,62–65 few data are available on activity factors that can be used to evaluate the relationship between time use or Inhalation Rates consumer product use and exposure to environmental agents In pregnant women, the amount of air breathed in or out during among pregnant and lactating women. normal respiration (i.e., tidal volumes) is inﬂuenced by hormonal Nethery et al.66 compared the time–activity patterns among a changes. Increasing levels of progesterone in the pregnant woman non-random sample of 62 pregnant Canadian women to the

Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 & 2014 Nature America, Inc. Changes during pregnancy and lactation Moya et al 455 Table 10. Mean (95% conﬁdence interval) time spent in various activities (h/day), by trimester.

Activity/location Pregnant cohort Pregnant cohort by trimester CHAPS comparison group

1st Trimester 2nd Trimester 3rd Trimester

At/near home 16.2 (15.7–16.8) 14.4 (13.3–15.4) 16.1 (15.3–17.0) 16.9 (16.0–17.8) 15.5 (14.7–16.3) Work 4.2 (3.6–4.7) 5.6 (4.4–6.7) 4.3 (3.5–5.1) 3.7 (2.8–4.6) 3.8 (3.0–4.6) Indoors, other 1.6 (1.3–1.8) 2.2 (0.9–3.6) 1.6 (1.3–1.9) 1.4 (1.1–1.7) 2.5 (1.9–3.0) Outdoors 0.3 (0.2–0.4) 0.0 (0.0–0.0) 0.2 (0.07–0.2) 0.4 (0.2–0.6) 0.6 (0.3–0.8) Car 0.9 (0.7–1.0 1.1 (0.5–1.7) 0.9 (0.7–1.1) 0.8 (0.6–1.0) 1.4 (1.1–1.7) Bus 0.2 (0.2–0.3) 0.3 (0.01–0.5) 0.2 (0.1–0.4) 0.2 (0.08–0.3) 0.1 (0.1–0.2) Walk 0.7 (0.5–0.8) 0.4 (0.2–0.7) 0.7 (0.6–0.9) 0.6 (0.4–0.8) 0.2 (0.1–0.2) Bike 0.1 (0.0–0.1) 0.02 (0.0–0.07) 0.06 (0.0–0.1) 0.06 (0.0–0.1) 0.0 (0.0–0.1) Abbreviation: CHAPS, Canadian Human Activity Pattern Study. Source: Nethery et al.66

Table 11. Activities associated with exposure to water, by pregnancy Table 12. Percentage of pregnant minority women reporting use of status. selected personal care products over a 48-h survey period. Deodorant 98 Characteristic Pregnant Not pregnant Lotion 82 (N ¼ 71) (N ¼ 43) Perfume 41 Liquid soap 29 Showering at home (%) 97.2 100.0 Hair gel 25 Showers per weeka (mean±SD) 7.1±2.8 7.2±2.4 Hair spray 10 Duration of showers (minutes) 13.9±5.2 13.9±6.0 Nail polish or polish remover 10 Bathing at home (%) 50.7 37.2 b Baths per week (mean±SD) 3.0±3.5 1.4±1.1 Source: Just et al.69 Duration of baths (minutes±SD) 28.8±12.9 41.3±30.3 Swimming (%) 25.4 27.9 c Swimming per week 1.3±1.6 0.6±0.5 countries (i.e., United Kingdom, Canada, The Netherlands, Norway, (mean±SD) and Australia). The results indicated that the percentage of women ± ± Duration of swimming (minutes) 73.9 46.1 80.8 79.3 who moved during pregnancy ranged from 9 to 32% Bathing children (%) 43.7 81.4 Washing dishes (%) 66.2 76.2 (median ¼ 20%). Four of the studies presented data by trimester Washing clothes (%) 14.1 21.4 and found that residential mobility was highest during the second Washing cars (%) 18.3 31.0 trimester. Other factors affecting mothers’ residential mobility Bathing pets (%) 18.3 11.9 included age (the probability of moving generally declined with age), socioeconomic status (mobility was generally higher among Abbreviations: N, number of observations. women with lower income), marital status (married women were Source: Zender et al.67 aAmong women showering at home. less likely to move), and parity (rates were generally higher in bAmong women bathing at home. women with fewer pregnancies). Relationships with factors such as cAmong women swimming. race, smoking, and alcohol use were more variable. Of the studies that reported on the distance moved, most distances were short, with median values that were typically o10 km. Bell and activities reported for 103 women in the Canadian Human Activity 68 Pattern Study (CHAPS). Changes in location-based activity patterns Belanger concluded that ‘‘residential mobility does not greatly were measured over the course of pregnancy. Table 10 provides inﬂuence exposure estimates, and presumably subsequent health risk estimates, due to the short distance of most moves.’’ the mean and 95% conﬁdence intervals for the pregnancy cohort 69 and the CHAPS comparison group. Just et al. conducted a survey among pregnant minority Zender et al.67 conducted a study in Colorado in 1996 and 1997. women to explore relationships between the use of personal care Its primary purpose was to compare tap water intake among products and exposure to phthalates. Consumer product use pregnant and non-pregnant women, but data on activities questionnaires were administered to study participants in the resulting in dermal contact with tap water (e.g., showering, third trimester of pregnancy. Data were collected for seven bathing, swimming, cleaning, etc) were also collected. A total of 71 product categories: deodorant, lotion or mist (spray application), pregnant and 43 non-pregnant women were recruited from Well perfume, liquid soap or body wash, hair gel, hair spray, and nail Infant and Children clinics. Table 11 shows the statistics for these polish or polish remover. Table 12 provides information on the activities. The results indicate that the frequency and duration of percent of participants using the personal care products over the showering was similar for pregnant and non-pregnant women, 48-h survey period. Deodorant was the product category with the but pregnant women spent more time bathing than non-pregnant most prevalent use (98%). However, when frequency of use was women. Table 11 also shows the percentage of pregnant and non- considered, liquid soap was used most frequently (mean of 3.4 pregnant women engaging in activities such as bathing children uses in 48 h), followed by lotion and deodorant. or pets and washing dishes, clothes, or cars. Bell and Belanger68 studied women’s residential mobility during Body Weight pregnancy and potential implications for environmental exposures The recommended weight gain during pregnancy is between 25 during pregnancy. Data from 14 studies on residential mobility and 35 pounds (11.5–16 kg) for normal-weight women.70 among pregnant women were examined for overall mobility rates Recommendations for weight gain are slightly higher in and distances moved. Seven of the studies were based in the underweight women and slightly lower in overweight and United States, whereas the remaining seven were based in other obese women. As the baby gains most of its weight during the

& 2014 Nature America, Inc. Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 Changes during pregnancy and lactation Moya et al 456 Table 13. Weight gained during pregnancy (kg), pre- and post Table 14. Weight gained during pregnancy (kg), for underweight, pregnancy body weight (kg), and post-pregnancy weight (kg) normal-weight, overweight, and obese women who had good retained. pregnancy outcomes.

Variable Mean±SD (range) Variable Mean±SD

Weight before pregnancy 59.7±9.7 (43.1–93.0) 1st Trimester Underweight 1.92±3.06 Weight gained during pregnancy Normal weight 2.19±3.47 1st Trimester 3.1±2.9 ( À 4.5–11.3) Overweight 2.16±3.95 2nd Trimester 6.4±3.0 ( À 6.8–13.6) Obese 1.65±3.94 3rd Trimester 6.5±2.9 (1.4–18.1) Total 16.2±5.2 (1.4–35.8) 2nd Trimester Underweight 0.57±0.20 Post-pregnancy weight Normal weight 0.58±0.22 0.5 months 67.2±1.0 (47.9–96.4) Overweight 0.51±0.24 2 months 65.5±1.0 (49.3–94.9) Obese 0.41±0.27 4 months 64.3±1.0 (48.6–3.2) 6 months 63.6±1.0 (47.2–94.2) 3rd Trimester 12 months 62.4±1.1 (44.4–96.0) Underweight 0.48±0.19 18 months 63.8±1.3 (47.8–98.4) Normal weight 0.51±0.21 Overweight 0.49±0.22 Retained weight, post-pregnancy Obese 0.47±0.24 ± 0.5 months 7.4 0.5 ( À 6.5–20.8) 73 2 months 5.8±0.4 ( À 5.1–16.8) Source: Carmichael et al. 4 months 4.7±0.4 ( À 5.8–15.5) 6 months 3.9±0.4 ( À 7.5–15.1) 12 months 2.5±0.5 ( À 8.3–13.5) mothers feeding their infants a combination of mother’s milk and 18 months 3.0±0.5 (10.1–14.5) formula. Dewey et al.41 evaluated weight loss during lactation among California women participating in the Davis Area Research Source: Janney et al.72 on Lactation Infant Nutrition and Growth study. Weight loss among 46 mothers who breastfed their infants was compared with weight loss among 39 mothers who fed their infants formula. last 2 months of pregnancy, it is recommended that women Weight loss among the two groups of women was similar at regulate their weight accordingly to gain most of their weight in 1 month postpartum, but the breastfeeding women weight losses the final months.71 However, reports indicate that only 30–40% of were greater than those of the formula-feeding group in women actually gain weight within recommended ranges.34 subsequent months (Table 16). Results were similar when weight Janney et al.72 evaluated pre- and post-pregnancy body weights was expressed as a percentage of the pre-pregnancy weight. At of 110 women in the Ann Arbor, Michigan area. The women 6 months postpartum, the breastfeeding group had an average ranged in age from 20 to 40 years and most were White body weight that was B2.8 kg lower than that of the formula- (106 Whites, 1 Asian American, and 3 African Americans). feeding group, and at 12 months the breastfeeding group had a Pre-pregnancy body weights were compared with postpartum mean body weight that was 3.2 kg lower than the formula-feeding weights at 0.5, 2, 4, 6, 12, and 18 months after parturition. Table 13 group. Over the first 12 months postpartum, breastfeeding presents data on weight gained during pregnancy, pre- and post- mothers lost 4.4 kg compared with 2.4 kg for the formula-feeding pregnancy body weights for the women, as well as information on mothers. Dewey et al.41 also found that greater parity and weight retained after pregnancy. As shown in Table 13, mean maternal height were associated with greater weight loss. body weight declined from 67.2 kg at 0.5 months after parturition Janney et al.72 indicated that women who bottle-fed their infants to 62.4 kg at 12 months after parturition. Carmichael et al.73 retained more weight over time than women who breastfed their provided similar data for a total of 7002 underweight, normal- infants, but ‘‘the effect of lactation on weight retention was weight, overweight, and obese-weight women in California, who sufficiently limited to warrant minimal emphasis on lactation as a had good pregnancy outcomes (Table 14). means of minimizing postpartum weight retention.’’ Factors such The US Environmental Protection Agency (EPA) analyzed the as age, marital status, and weight gained during pregnancy were body weight data for 1248 pregnant women from the 1999–2006 important contributors to postpartum weight losses. Women who NHANES.35 Mean body weights by trimester were as follows: 76 kg were older, unmarried, or had greater weight gain during for the first trimester, 73 kg for the second trimester, and 80 kg for pregnancy were found to retain more weight over time.72 the third trimester. The statistically weighted average body weight of all pregnant women was 75 kg. It should be noted that the first trimester mean body weight reported in US EPA35 was influenced DATA GAPS AND DISCUSSION by a few high body weights with high sample statistical weights Women undergo a wide array of physical and behavioral changes (Table 15). On the basis of an analysis of 1999–2006 NHANES data during pregnancy and lactation. Although not all of these from the general female population, mean body weights for all changes create opportunities for new or different environmental women, ages 16 to o50 years, ranged from 66 to 77 kg.35 exposures, some may increase or decrease exposures to environ- There are many confounding factors that impact postpartum mental contaminants. The purpose of this paper is to provide body weight change.74 For example, lactation has been shown to an introduction to the topic of pregnancy and lactation exposure- have a role in the rate of post-pregnancy weight loss, but such related changes. Although a more systematic and comprehensive losses are influenced by the length of time over which lactation review of the literature may be warranted, this effort is intended to occurs. Brewer et al.75 examined postpartum weight changes in 56 summarize some of the data on exposure factors for this Louisiana women. Overall, there was a steady, significant decline population and highlight areas where data gaps exist. in weights. Weight losses averaged 8.30 kg for the breastfeeding Some information is available on exposure factors for pregnant group, 8.19 kg for the formula-feeding group, and 7.22 kg for the and lactating women. However, many of these studies were

Journal of Exposure Science and Environmental Epidemiology (2014), 449 – 458 & 2014 Nature America, Inc. Changes during pregnancy and lactation Moya et al 457 Table 15. Estimated body weights (kg) of pregnant women—NHANES (1999–2006).

Trimester Sample size Mean SD Percentiles

5th 10th 15th 25th 50th 75th 85th 90th 95th

1 204 76 3 48 50 55 60 74 91 98 106 108 2 430731505357617283939598 3 402 80 1 60 63 65 69 77 88 99 104 108 Ref/Dka 1866924652556065778487108 All 1222 75 1 50 55 59 63 73 85 94 99 107 Source: US EPA.35 aPregnant women who either refused to tell which trimester they were in or did not know, or data were missing.

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