Environmental Contaminants in Breast Milk
Krista Nickerson, CNM, MSN
J Midwifery Womens Health. 2006;51(1):26-34. ?2006 Elsevier Science, Inc.
Abstract and Introduction
Toxic environmental contaminants can be transferred from mother to infant via breastfeeding. Persistent organic pollutants (POPs) are a family of lipophilic stable chemicals that bioaccumulate in adipose tissue and create a lasting toxic body burden. Breastfeeding provides a significant source of exposure to POPs early in human life, the effects of which are unknown, and is the subject of a growing body of research. Despite the possibility of harm from environmental contaminants in breast milk, breastfeeding is still recommended as the best infant feeding method. This article reviews what is known about POPs in breast milk and their effect on infant development to inform clinicians about the issue, provide recommendations for practice, and promote environmental and public health policies that reduce human exposure to harmful pollutants.
We are what we eat. The interconnectedness of humans with their environment is illustrated by this familiar maxim. Substances that enter the human body from our external environment—food, water, and air—are the
source for our biologic composition. Now imagine the breastfeeding maternal-infant dyad. A mother's body becomes the environment for her children throughout pregnancy and through breastfeeding. Over the past several decades, the public has grown increasingly aware that chemicals in the environment are entering our bodies and sometimes causing harm. Recently, this awareness has extended to concern about what effect(s) toxic contaminants have on breastfeeding women and their children. The issue of environmental pollution and breastfeeding was brought to light by Sandra Steingraber, a mother and an ecologist, an author and public spokesperson in 2001. Her book Having Faith: An Ecologist's Journey to Motherhood has fueled a growing concern over this issue. It is a fascinating and well-researched personal account of her own pregnancy,
birth, and breastfeeding experience, emphasizing the environmental influences on her own developing child. In a recent issue of the popular magazine Mothering, the lead article addressed breastfeeding and
environmental contaminants. Newspapers, radio programs, and other mainstream media are bringing this particular issue to the lay public. Obstetric providers need to recognize and confront the issue of pollutants in breast milk for several reasons. 1) As clinicians, we need to be aware of the research and guidelines promoted by leading experts to counsel our clients appropriately. 2) As caretakers of women's reproductive health, we need to promote progressive public health policy concerning this issue to prevent future harm.
The benefits of breastfeeding are clear. Breast milk is nutritionally balanced and biologically appropriate for human infants. The species-specific components present in breast milk protect infants against infections; promote immune and neurologic system development; and may decrease the risk of disease, including allergies, obesity, insulin-dependent diabetes mellitus, inflammatory bowel disease, and sudden infant death syndrome (SIDS). Breastfeeding also facilitates maternal-infant
attachment. However, there is unambiguous data that breast milk accumulates and harbors persistent organohalogens, including persistent
organic pollutants (POPs), heavy metals, and volatile solvents. The effect
of these contaminants on the breastfeeding infant is the subject of a growing body of research. As a category of pollutants, POPs include chemicals that can be very toxic to humans, are found in relatively high quantities in breast milk, and have been fairly well studied. Although all breast milk contaminants are important to consider, this article focuses on the evidence about the effects of POPs in breast milk.
Persistent Organic Pollutants (POPs)
POPs are a family of chemicals manufactured either for a specific purpose (e.g., pesticides or flame retardants in electrical equipment or furniture) or produced as by-products of incinerated waste. Current and historic industrial emissions have deposited POPs into the air, soil, and water, where they find their way into the food chain. POPs are very stable compounds that are not readily degraded in the environment nor completely metabolized or excreted by organisms. As they are consumed and stored by one organism after another, these substances
bioaccumulate in the food chain. Because humans are at the top of the food chain, we accumulate these chemicals over time, collecting what is referred to as a lifetime body burden. POPs are now ubiquitous but usually low-level contaminants in human beings worldwide. Although certain
nations have banned particular POPs, their existence is not confined to
areas of use, as distribution occurs through atmospheric and oceanic transfer, as well as through food sources. Even when production of these chemicals is halted, continued long-term exposure is certain. The POPs family includes dioxins, which commonly refers to polychlorinated dibenzodioxins (PCDD) and polychlorinated
dibenzodifurans (PCDF), as well as polychlorinated biphenyls (PCBs), polybrominated biphenyls (PBB), polybrominated diphenyl ethers (PBDE), and other organochlorine pesticides such as
dichlorodiphenyltrichloroethane (DDT) and hexachlorobenzene ( Table 1 ).
Polychlorinated Biphenyls (PCBs)
The PCB subfamily consists of 209 different chemicals. They were first produced in the United States in the 1930s as insulators in electrical equipment, and for paint, carbonless copy paper, and pesticides until they were banned in 1977; however, production continues elsewhere. In industrialized nations, where the majority of PCBs have been manufactured, they are probably the most widespread and critical organochlorine contaminants in human milk. The levels of PCBs in the breast milk of Europeans and North Americans are generally higher than those of women in nonindustrialized nations. Their presence can be
detected in meat and fish. Numerous advisories concerning freshwater fish consumption due to PCB contamination have occurred in the United
States. In 1981, 93% of breast milk samples in one study exceeded the US Food and Drug Administration's limit for newborn ingestion of PCBs in mg/kg body weight.
The dioxin subfamily consists of 75 PCDDs and 135 PCDFs, 17 of which
have been detected in humans. Dioxins are by-products of the production
and combustion of chlorinated compounds, which include the manufacture of pesticides, paper bleaching, and incineration of waste. They usually occur as collections of several different dioxin compounds. The toxicity of PCBs and dioxins can be difficult to measure because of heterogeneous occurrence and is commonly referred to in toxic equivalencies, which refer to the degree that a particular sample of multiple compounds resembles
the bioactivity of the most toxic dioxin. Dioxins have been studied in at
least 36 countries, and like PCBs, levels of dioxins are higher in more industrialized countries. Time trend data suggest that breast milk levels of dioxins are decreasing in many countries; however, for some, including the United States, the data are too ambiguous to make definite conclusions.
These results suggest that efforts to reduce emissions have notable effects.
The main source of environmental exposure to dioxins is through food of animal origin, such as meat, dairy products, and fish.
Polybrominated Diphenyl Ether (PBDE)
PBDE is a flame retardant widely used in electrical appliances, foam, and textiles for furnishings. Its use is still unrestricted, and it is found in increasing levels in breast milk. PBDEs have a similar structure to PCBs
and have similar properties. However, they are thought to be more susceptible to environmental degradation. That withstanding, levels of PBDE in human milk samples from American women are 10 to 100 times higher than European levels.
Organochloride Pesticides: DDT and DDE
Organochloride pesticides include DDT, hexachlorobenzene, hexachlorohexane, chlordane, dieldrin, and heptachlor, among others. DDT is a well-known agricultural insecticide that has been used extensively for over 40 years. It was banned in many countries, including the United States in 1972, but it is still used in other nations, such as Mexico, for control of malaria-carrying mosquitoes.
Dichlorodiphenylchloroethane (DDE) is a toxic metabolite of DDT that has estrogenic properties. Levels of DDT and DDE in human milk have
decreased in areas where cessation of its use has occurred. The other
organochloride pesticides have been used as agricultural and domestic pesticides and fungicides but are now banned in the United States
because of their toxicity and biologic persistence. However, their use in
other countries continues, and their existence is still detected in breast milk, although levels have decreased.
Breastfeeding Exposure to POPs in Infants:
Pharmacokinetics and Body Burden
The pharmacokinetics of POP transfer from mother to infant via breastfeeding is a complex process that is strongly influenced by a particular chemical characteristic of all POPs—their distinct affinity for fat.
POPs are lipophilic by nature. When consumed, they bioconcentrate in adipose tissue, and because of their long half-life, POPs accumulate with age and exposure. These chemicals remain in fat storage, making up the organism's lifetime body burden, while minute amounts circulate in serum. Excretion of POPs occurs either very slowly through stool or more quickly through lactation. Figure 1 illustrates the pathway of POPs excretion in the body of a lactating woman. The half-life of dioxins in adults is
approximately 4.2 to 5.6 years. Although pregnancy exposes the fetus to
minor amounts of POPs carried in serum and transferred via the placenta,
[14,16]a more significant exposure occurs through breastfeeding.
Pathways of transition for persistent organic pollutants in lactating women. Adapted with permission from Jensen.
(Figure by C. Byrne).
Lactational physiology exerts a unique influence on the kinetics of POPs. When a woman begins lactating, her fat stores are mobilized to efficiently excrete lipids and their trailing POP partners in breast milk. She effectively transfers her own body burden of pollutants to her newborn. The lipid
content in breast milk may have concentrations of POPs 10 times higher than lipids of ordinary food.
Levels of POPs in human milk formula are minimal to none. Although formula is derived mostly from cow's milk, the milk fat is replaced by vegetable oils, which are usually free of these contaminants. In a study of 246 preschool children in Michigan, the serum PCB level in formula-fed children was 0.3 ? –0.7 ng/mL, compared to 5.1 ? 3.9 ng/mL in children who were breastfed for at least 6 months. Postnatal exposure via
breastfeeding is the principal determinant of body burden levels during early childhood, is significantly correlated with maternal levels, and shows [16-18]a dose-dependent relationship based on length of breastfeeding.
Several different pharmacokinetic models of estimating infant body burden [17,19]due to breastfeeding have been proposed. Some models have been
used to estimate the extended effect of breastfeeding on infant lifetime body burden or on the toxicologic potential of the body burden. These
models include factors such as maternal body burden levels and lactation-dependent changes, milk composition, length of breastfeeding, transfer kinetics, and metabolism of the chemical. The daily dioxin intake of breast-fed infants may be as high as 80-fold higher than in adults. Others have
estimated that by adulthood, breastfed individuals will accumulate a dose
3% to 18% higher than individuals who were not breastfed. To the
contrary, another model predicts that breastfed and nonbreastfed individual body burdens will eventually equalize by the age of 10. The
various methods of producing these estimates have been scrutinized, and they remain merely estimates and best guesses based on the available information.
A mother's body burden of POPs is dependent on several factors. Background exposure is derived mostly from low-level food and water contamination. Important factors for women with normal background exposure (i.e., no acute episodes of high exposure) seem to be age and
previous lactation. Age is an indicator of exposure level because the passage of time allows for continued accumulation of pollutants. Older nulliparous women are expected to have higher body burdens. However, [10,22]previous lactation is associated with lower POP levels in breast milk.
Researchers have estimated that maternal PCB/dioxin body burden decreases as much as 20% to 70% during 6 months of exclusive [17,22]breastfeeding. Thus, over the course of her childbearing years, a mother will transfer more POPs to her first child, with decreasing amounts to subsequent children.
Geographic location influences body burden of POPs based on proximity to agricultural use of chemicals, waste incineration sites, and other factors. For example, Inuit women have the greatest body burden known to occur from general background environmental exposure, secondary to climate
factors and a diet of lipid-rich sea mammals. The accumulation of POPs
in the arctic environment, far from their original site of production and use,
is via long-distance atmospheric and oceanic transport.
Other determinants of exposure that influence maternal body burden to varying degrees include diet, cigarette smoking, urban living, and occupation. It is generally agreed that food represents the main source
(over 90%) of environmental exposure to dioxins and PCBs. Within the
diet, animal products (dairy, meat, and fish) appear to contain the highest amounts of dioxins/PCBs, because of their accumulation in fat. Therefore, a vegetarian diet appears to be associated with lower serum dioxin levels. However, short-term dietary regimens with a low PCB/dioxin intake do not reduce breast milk levels. Consumption of freshwater sports fish conveys a higher level of PCBs in breast milk. Cigarette
[7,22,26]smoking increases levels of DDE, PCBs, and hexachlorobenzene.
Finally, breast milk PCB levels differ according to occupation; students and professionals have higher levels than laborers and farmers. Neither
education nor body weight seems to affect PCB or DDT levels; however, weight loss seems to concentrate dioxin levels in body fat.
Health Outcomes of POP Exposure in Infants
Extensive laboratory and animal research has shown that POPs have a significant effect on the biochemical processes and function of several organ systems. Although these studies are immensely important to the science of toxicology, this review focuses on human studies only. Because human research is more methodologically and ethically complex, fewer studies are available, and their results are harder to interpret. In general, the question is not whether there are adverse effects, but rather, are adverse effects occurring at the existent levels of exposure? For example, although minor changes in motor function or memory may be insignificant to the individual child, the idea that a portion of children in the general population are noted to be affected by using insensitive methods of detection is worrisome. All of the evidence provided here concerns levels of contaminants that are found in human populations at normal exposure levels.
Infancy is a unique developmental period in the human life span. During this stage, the immunologic, neurologic, and reproductive systems are functionally immature, and the infant undergoes rapid tissue growth and development. In addition, this development necessitates a larger quantity of calories per body weight and increased fat consumption via breast milk or formula. These factors create potential for significant systemic effects, whether beneficial or detrimental. The research on health outcomes of
perinatal exposure to POPs has focused on the endocrine, reproductive, immune, and neurologic systems.
It is important to acknowledge the difficulty in distinguishing effects that may be associated with in utero toxic exposure versus those that are from breastfeeding. In utero exposure to POPs does occur to a much lesser degree. However, because of increased vulnerability during fetal development, the impact of the smaller exposures during pregnancy may surpass the infinitely larger exposure to POPs in breast milk. The research involving the health effects of POP exposure through breastfeeding does not always control for the possibility of teratogenic exposure to POPs during gestation. These differences will be elucidated where studies have distinguished between the two.
Growth and Endocrine-Related Events
Preliminary evidence regarding overall growth has shown that in utero exposure to PCBs may cause low birth weight; however, there is contradictory evidence regarding breastfeeding exposure and weight gain [14,28]in infancy and early childhood. Several studies have looked at pubertal
[29,30]growth and perinatal exposure to PCBs and DDE. All of them have
found that prenatal exposure to PCBs may cause an increase in body size at puberty for girls. However, no relationship was seen with lactational exposure.
Less evidence is available on POPs and reproductive outcomes. Animal studies have clearly linked PCBs and dioxins to reduced sperm count and fertility, endometriosis, and altered sexual development and behavior.
However, very few human studies have been completed. Perinatal exposure to PCBs and DDE did not seem to affect pubertal development, [29,30]as measured by Tanner stages and age of menarche. On the other hand, Michels-Blanck et al. completed a study of 327 girls whose
mothers, affected by an industrial accident, were exposed to high levels of PBBs through animal and dairy products. It was found that perinatal PBB exposure led to a decrease in the age of menarche and earlier pubic hair development in the girls born to mothers who were exposed. The study was unable to distinguish prenatal from postnatal exposure. The postulated mechanism for such effects is via endocrine disruption and/or estrogenic activity of the various POPs.
POPs may also disrupt the endocrine process of lactation itself. Gladen and Rogan and Rogan et al. investigated the role of DDE and PCBs on
the duration of lactation in three communities in North Carolina and one community in Mexico. Levels of DDE and PCBs were measured in the milk of lactating women and compared with their reported duration of lactation. Higher levels of PCBs and DDE in breast milk were associated with
decreased duration of lactation, despite adjustments for potential confounders and biases. The authors concluded that DDE and PCBs may affect women's ability to lactate, suggesting that the chemicals' estrogen-like effects may inhibit the process. In another study, milk volume was found to be inversely related to PCB body burden.
Additional preliminary evidence indicates that perinatal exposure to PCBs and dioxins may disrupt thyroid hormone regulation; however, the data are [30,34]contradictory. Inconsistencies may be related to different methods of study, as well as the presence of multiple confounding factors. Koopman-
Esseboom et al. studied 105 maternal-infant pairs and found that higher levels of dioxins and PCBs correlated with significantly lower plasma levels of maternal total triiodothyronine and total thyroxine and with higher plasma levels of TSH in the infants in the second week and third month after birth. However, direct, isolated measurements of thyroid hormone levels may not be the most sensitive indicator of a perturbation of thyroid hormone metabolism. It is well documented that thyroid hormone regulation has a profound effect on neurologic development; therefore, any disturbance has the potential for adverse effects.
The research concerning neurodevelopmental effects of PCB and dioxin exposure is both more extensive and more consistent than research on growth and endocrine development. Although breastfeeding exposure to PCBs and dioxins occurs to a much greater degree than prenatal exposure, it appears that prenatal exposure has a more measurable effect on neurodevelopmental outcomes. Prenatal exposure to PCBs has been associated with hypotonicity and hyporeflexia in newborns; poorer psychomotor performance at 3, 6, and 12 months; poorer cognitive functioning at 42 months; poorer mental and motor development
between 7 and 42 months; and poorer short-term memory function at 4 years. Several of these studies had inconsistent results and did not find significant effects in every area or age group tested. Meanwhile, despite the high PCB and dioxin levels transferred via breast milk, breastfeeding seemed to have a beneficial effect on neurologic status compared with [36,38]formula feeding. Other factors present in breast milk may have a
protective effect on normal neurologic development. However, when comparing only breastfed infants and ignoring their formula-fed counterparts, the deleterious effects of higher levels of POPs in breast milk reappears. Walkowiak et al. found that mental and motor development
between 7 and 42 months of age has a significant negative association with PCB concentration in early human milk but not in cord blood samples.
There are several limitations to the research on neurodevelopment scores. One particular difficulty in studying older children is that factors such as the home environment and maternal IQ become more significant variables that [36,39]affect development as a child ages. Both human and animal studies
have demonstrated that POPs and other contaminants rarely occur individually, and the effects of these chemicals are quite complex, as are the neurodevelopmental processes of humans. Global functioning tests may not be able to distinguish deficits of one particular domain, because they will be masked by the inability of the test to discriminate between global functioning and specific cognitive functions.
There are very few studies concerning perinatal exposure to POPs and their effect on the immune system. Moreover, the immune-supporting properties of breast milk are well known and have a beneficial effect on infants, which may mask any harmful influence of POPs. Weisglas-Kuperus et al. investigated the effect of prenatal and postnatal PCB levels on the prevalence of infectious diseases. They measured humoral immunity to antibodies after vaccination and measured immunologic markers in children at 42 months. Results demonstrated that prenatal PCB exposure was associated with lower antibody levels to mumps and measles after vaccination and significant changes in T-cell markers, indicating a greater susceptibility to infectious diseases. High current PCB levels were associated with a higher prevalence of recurrent middle ear infections and chicken pox and lower prevalence of allergic reactions. Increased dioxin levels were associated with higher prevalence of coughing, chest congestion, and phlegm. It is of interest that the negative effect of high postnatal PCB level was counteracted by the positive effect of longer duration of breastfeeding. DeWailly et al. measured levels of 10
PCB congeners and 8 different organochlorine pesticides or metabolites in the breast milk of 213 Inuit women and the chemicals' relation to serum immunologic parameters and occurrence of otitis media in the women's infants. The study found that immunologic parameters did not differ between breast and formula-fed infants, nor was there an association between the milk levels of the pollutants that were assessed and immunologic parameters in the infants. On subanalysis, DDE and hexachlorobenzene levels in breast milk were positively associated with occurrence of otitis media within the first year of life.