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To breastfeed or not to breastfeed: a review of the impact of lactational exposure to polychlorinated biphenyls (PCBs) on infants.

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Introduction

Polychlorinated biphenyls (PCBs) are a family of 209 synthetic hydrocarbons once extensively used in a variety of industrial applications as coolants or lubricants. PCBs are ubiquitous environmental contaminants with a tendency to bioaccumulate up the food chain and sequester in human adipose tissue. PCBs readily transfer across the placenta, but perinatal exposure is believed to occur predominantly in the postnatal period through breast milk (Jacobson, Fein, Jacobson, Schwartz, & Dowler, 1984). Surveys of breast milk show widespread prevalence of PCB contamination worldwide, especially in industrialized countries (Jensen, 1983; Rogan et al., 1986). Breast milk concentrations of PCBs tend to be higher than those in adult diets and their toxic effects in children may be more severe and affect more organ systems than in adults (Guo, Lambert, & Hsu, 1995). Depending on the duration of breastfeeding, estimates suggest that a breastfed infant may accumulate lifetime exposure that is 3% to 18% higher than that of a formula-fed infant (Lorber & Phillips, 2002). These problems with PCBs, coupled with their lipophilic character and poor biodegradability, led to concerns regarding the safety of breastfeeding infants. The purpose of this article is to provide an overview of the known health effects of PCBs in children, examine the level of evidence with regards to the risk of postnatal exposure via breastfeeding, and offer recommendations.

Methods

Studies considered for this analysis included peer-reviewed articles (1966-2007) using the PUBMED database of the U.S. National Library of Medicine. Search terms included "polychlorinated biphenyls (PCBs) and routes of exposure," "PCBs and infant outcomes," "PCBs and breastfeeding," "PCBs and infant growth," "PCBs and infant development," and "adverse effects of PCBs in children." Subsequently, the reference sections of articles were examined for additional relevant articles. Articles were required to be full text manuscripts and to be written in the English language. Qualifying articles were reviewed and evaluated for related content. Of 107 articles retrieved, 58 were included in this review.

Results

Neurological Effects of PCBs in Children

The effects of PCBs on infant neurological development have been extensively studied. These effects are influenced by mode of exposure (transplacental or lactational) and age of the child at the time of assessment, with consequences being more evident in early life. Jacobson and co-authors (1984) tested 242 neonates whose mothers consumed PCB-contaminated fish from Lake Michigan and compared them with 71 control infants whose mothers did not eat fish during pregnancy. They reported motoric immaturity, limited lability, and hypoactive reflexes on the Brazelton Neonate Scale among infants in the study group on postpartum day three. These findings have been corroborated by others (Rogan et al., 1986). Higher breast milk levels of planar PCBs in particular were associated with hypotonia (Huisman et al., 1995). A prospective study of 802 infants found that although higher transplacental exposure to PCBs was associated with lower Bayley psychomotor scores at 6 and 12 months of age, such an association was not present in children exposed to PCBs or dichloroethane (DDE) via breast milk (Gladen et al., 1988).

The effect of PCBs on neurological development in older age groups is not as explicit. Rogan and Gladen (1991) found that children in the top fifth percentile of transplacental exposure to PCBs had adjusted scores for development that were four to nine points lower than their peers. The authors failed, however, to detect similar results with DDEs and with exposure to PCBs via breastfeeding. A similar Dutch study discovered that higher in utero exposure to PCBs decreased psychomotor scores at three months of age and lactational PCB and dioxin exposure negatively affected scores at seven months of age (Koopman-Esseboom et al., 1996). Preadjustment, breastfed infants scored significantly higher on the psychomotor score at seven months of age, compared with formula-fed infants. This advantage was eliminated by lactational exposure to PCBs and dioxins, becoming comparable to the psychomotor score of the formula-fed infants. Neither PCB and dioxin exposure nor feeding type had any effect on development at 18 months of age.

Long-term effects of perinatal exposure to PCBs and dioxins on neurological and cognitive development continue to be studied. Boersma and Lanting (2000) followed a cohort of 418 infants from birth to six years of age with assessments at 18, 42, and 72 months of age. Prenatal exposure to PCBs and dioxins was shown to negatively affect neurological optimality scores at 18 months and cognitive development at 42 and 72 months. No effect was demonstrated by postnatal exposure to the measured pollutants via breast milk. In fact, despite higher PCB exposures from breast milk, a beneficial effect of breastfeeding was demonstrable, with improved fluency of movements and cognitive development tests among children with history of lactational exposures. The authors concluded that prenatal exposure to PCBs has subtle negative effects on neurological and cognitive development of the child up to school age. In Michigan, a group of four-year-old children who had been breastfed for more than one year by mothers with above-aver age breast milk PCB levels was also found to have reduced activity (Jacobson, Jacobson, & Humphrey, 1990).

Evidence exists that long-lasting cognitive and behavioral damage may persist up to adolescence in children with high levels of prenatal PCB exposure. This damage may include mild cognitive deficit in children up to at least 16 years of age, lower IQ scores, and higher likelihood of being at least two years behind in reading comprehension than their peers with less exposure (Jacobson & Jacobson, 1996; Lai et al., 2002). These findings were not universally compatible with other investigations, however. For example, Gray and co-authors (2005) found that in utero exposure to background levels of PCBs was not associated with lower IQ at age seven.

PCBs and Fetal Growth Outcomes

Concerns about consumption of fish from PCB-polluted bodies of water have encouraged research focusing on adverse birth effects among women with such dietary exposures. Although the major concern may relate to neurotoxicity, numerous published studies examined fetal growth outcomes, e.g., preterm birth, low gestational age, and low birth weight. Higher levels of PCBs and organochlorine compounds have been found in women with miscarriages than in women with a normal course of pregnancy (Leoni et al., 1989; Saxena et al., 1981). In one study after adjusting for confounders, PCB exposure was related to both lower birth weight and smaller head circumference (Fein, Jacobson, Jacobson, Schwartz, & Dowler, 1984). These findings were replicated by a Swedish study in which an increased risk of low birth weight was observed among infants born to mothers who reported a high intake of fish from the Baltic Sea (Rylander, Stromberg, & Hagmar, 1996).

A number of investigators have reported findings that are at variance with the above studies. Dar and co-authors (1992) found that birth size was positively associated with PCB exposure for most mothers. A recent cohort study also failed to demonstrate an association between maternal lifetime consumption of fish from Lake Ontario and reduced birth size as indicated by weight, length, and head circumference (Buck et al., 2003). Another study of birth outcomes among a cohort of mothers with a history of occupational PCB exposure reported a negative association between PCB exposure and infant birth weight, which disappeared after adjusting for gestational age and other variables (Taylor, Stelma, & Lawrence, 1989). Grandjean and co-authors (2001) concluded that no evidence exists of a PCB-exposure-associated decrease in birth weight among their study group of singletons born to 182 women from the Faroe Islands. The inconsistency in these studies has been explained in part by the possibility that the potential adverse effects of seafood contaminants such as PCBs may be balanced by the beneficial effect of seafood consumption during pregnancy (Guldner, Monfort, Rouget, Garlantezec, & Cordier, 2007).

PCBs and Childhood Growth

The lack of agreement regarding effects of PCB exposure on birth weight extends to postnatal growth patterns. Some studies have reported that in utero PCB exposure was associated with lower birth weight and lower postnatal growth rate (weight, length, and head circumference) from birth to three months of age (Jacobson et al., 1990; Patandin, Koopman-Esseboom, de Ridder, Weisglas-Kuperus, & Sauer, 1998). This finding did not extend, however, to lactational PCB and dioxin exposure in breastfed children.

Human data related to the association between PCBs and later growth and development, such as during puberty, are sparse and inconsistent. In 1978 in Taiwan about 2,000 people were poisoned after ingesting cooking oil contaminated with heat-degraded PCB (the "Yucheng" incident). A total of 118 children born to Yucheng women between 1978 and 1985 and their matched nonexposed controls were identified in 1985 and have been followed ever since (Rogan et al., 1988). This cohort has continued to be a valuable source of information on adverse outcomes associated with PCBs (Hsu et al., 1985). An initial assessment of 49 Yucheng newborns delivered between 1979 and 1985 found that they weighed 500 g less at birth than their age-matched controls (Lan, Yen, Yang, Yang, & Chen, 1987). Follow-up examination several years after showed a persistent delay in growth at age six months-seven years (height and weight) and 6-13 years (height) (Guo, Lin, Yao, Ryan, & Hsu, 1994; Rogan et al., 1988). Another accidental food contamination event in Michigan in 1973 led to the exposure of more than 4,000 individuals to polybrominated biphenyls (PBBs). Blanck and colleagues (2002) examined the association of estimated PBB and PCB exposure during pregnancy with current height and weight in 308 daughters (mean age: 15.2 years) born to women in that cohort. No association was found between prenatal PBB exposure and either daughter's current height or weight adjusted for height. Prenatal PCB exposure above 5 parts per billion, however, was associated with reduced weight adjusted for height (Blanck et al., 2002).

By contrast, a positive effect of PCB exposure on growth has been reported in the literature. A study from North Carolina found that girls with the highest transplacental PCB exposure were heavier for their height than other girls by 5.4 kg (Gladen, Ragan, & Rogan, 2000). In the case of boys their height at puberty increased with transplacental exposure to DDE, as did their weight adjusted for height. These findings are in agreement with other investigators (Hertz-Picciotto et al., 2005; Rogan et al., 1987).

Sexual, Endocrine, and Reproductive Effects of PCBs

The effects of PCBs or polychlorinated dibenzofurans/dibenzodioxins (PCDFs) and related compounds on sexual maturation, endocrine, and reproductive functions have been extensively studied. These compounds alter sexual maturation and endocrine function in animals (Brouwer et al., 1999; Hany et al., 1999). Evidence is emerging that similar effects occur in humans. A study of the Yucheng children cohort (described earlier) found that boys with prenatal exposure to PCBs had reduced penile length, but testicular volume and pubertal stages were unaffected (Guo et al., 1995). Yucheng girls, by contrast, did not show any apparent delays in sexual maturation. A follow-up investigation of the Yucheng girls was conducted when they were 13-19 years old. The results of that study suggested that prenatal PCB/PCDF exposure was associated with unchanged age at menarche, higher serum estradiol/ FSH levels in the follicular phase of menstrual cycle, and shortened menstrual cycles (Yang et al., 2005). Women in Japan who were victims of a poisoning incident similar to the Yucheng event (Yusho) in 1968 exhibited similar findings. The women in the Yusho cohort were found to have irregular menstrual cycles and low urinary excretion of estrogens, pregnanediol, and pregnantriol (Tsukamoto, Makisumi, & Hirose, 1969). They also demonstrated an increased risk of induced abortion and preterm birth within the first 10 years after exposure.

A study in Michigan of females with a history of higher prenatal and lactational exposure to a related group of chemicals (PBBs) revealed an earlier age at menarche and earlier pubic hair development among breastfed girls (Blanck et al., 2000). The authors did not find, however, an important association between PCB exposure and age at menarche or Tanner stage. These findings are consistent with Gladen and co-authors (2000), who reported that transplacental or lactational exposure to PCBs had no effect on age at which pubertal stages were attained. In another study of women exposed to dioxins (TCDD) following an industrial accident in Seveso, Italy, in 1976, premenarcheal exposure was associated with prolonged menstrual cycle (Eskenazi et al., 2002). Such effects, however, were not observed in women exposed after menarche. Significant gaps remain in our understanding of the complex interactive mechanism of biological actions of PCBs and the specific factors responsible for their reproductive toxicity (Kumar, 2004).

Adverse Immunological Effects of PCBs

The immune system of the developing fetus and the newborn is particularly vulnerable to the toxic effects of chemicals (Tryphonas, 1998). Although studies of perinatal PCB exposure and immune function in children are sparse and fairly recent, indications of altered immune status in exposed children appear to be well established. A study of children born to women who were highly exposed to PCBs and PCDFs in the Yucheng incident found a higher incidence of respiratory symptoms during the first six months of life and of otitis media at school age (Chao, Hsu, & Guo, 1997; Rogan et al., 1988). Dallaire and co-authors (2006) reported similar findings of a positive association between cord PCB-153 blood levels of 343 Inuit children and the incidence of acute middle ear and lower respiratory tract infections. A Dutch study of 207 preschoolers similarly showed that prenatal exposure to PCBs and dioxins was associated with an increase in T cell lymphocytes, a higher prevalence of recurrent otitis media and of chickenpox, and a lower prevalence of allergic reactions (Weisglas-Kuperus et al., 2000). The negative effect of PCB exposure on the prevalence of recurrent otitis media and chickenpox and of allergic reactions was counteracted by the positive effect of duration of breastfeeding. A separate effect of lactational PCB exposure was also evident; children with higher postnatal exposure through breast milk had a higher prevalence of recurrent middle ear infections. The authors also successfully demonstrated that the effect of postnatal PCB exposure on recurrent otitis media persisted into later childhood (Weisglas-Kuperus, Vreugdenhil, & Mulder, 2004).

Perinatal exposure to PCBs has also been shown to adversely impact immune response to routine childhood immunizations. A study of two birth cohorts in the Faroe Islands (a population with elevated dietary exposure to PCBs), found that the antibody response to diphtheria vaccine decreased by 24% at 18 months of age and to tetanus toxoid by 17% at seven years of age for each doubling of the cumulative PCB exposure (Heilmann, Grandjean, Weihe, Nielsin, & Budtz-Jorgensen, 2006).

Breastfeeding and PCBs

The concerns regarding the safety of breastfeeding are legitimate, considering the tendency of PCBs to bioconcentrate in maternal milk and the potential for infant exposure to be as much as a 50-fold higher dose per kilogram of body weight than the average adult (Patadin et al., 1999). Despite this, the scientific literature shows that breastfed infants continue to fare better than their formula-fed peers and evidence is insufficient to support advocating that mothers not breastfeed their infants. The American Academy of Pediatrics has concluded that the risks posed by PCBs in breast milk are outweighed by the benefits of breastfeeding.

It is appropriate to discuss issues related to postnatal PCB exposure assessments in infants at this point. Postnatal assessment of PCB exposure is challenging because of the difficulty in obtaining sufficient plasma samples to perform PCB analysis (Ayotte et al., 2003). Therefore, researchers commonly use the concentration of PCBs in breast milk multiplied by duration of breastfeeding to estimate postnatal exposure (Koopman-Esseboom et al., 1996; Walkowiak et al., 2001). But the correlation between prenatal and lactational exposures makes it difficult to separate their effects completely (Gladen et al., 2000). Infants with high prenatal exposures are likely to have high lactational exposures as well. Investigators have been able to mitigate this problem to some extent by stratifying infants on the basis of exclusively breast fed or formula fed. A total of six human longitudinal studies examined the effects of PCBs in human milk using this approach (Jorissen, 2007).

Gladen and colleagues conducted studies in North Carolina in 1988 and 2000 to ascertain the impact of breast milk and transplacental PCB and DDE exposures on neurological development (discussed earlier). Lactational exposure to either of the two chemicals was not associated with changes in scores on the Bayley Scales of Infant Development at 6 and 12 months of age (Gladen et al., 1988). The authors concluded that given the beneficial effect of breastfeeding on neurological development, the attenuation of benefits may represent a significant insult. They were not the first to arrive at this conclusion, however. This statement was first documented by Koopman-Esseboom and co-authors (1996), who set out to evaluate the effects of in utero and lactational exposure to PCBs on mental and psychomotor development of Dutch infants (discussed earlier). They found that although PCB exposure via breast milk had no effect on Bayley Psychomotor Development Index scores at 3 and 18 months of age, total PCB toxic equivalent modified the positive association between breastfeeding and PDI scores at seven months. A subsequent follow-up study of the North Carolina cohort in 2000 examined the impact of in utero and breast milk exposures to PCBs on growth and sexual maturity. The investigators failed to demonstrate a significant relationship between PCB exposure via breast milk and physical growth or sexual maturity, even though they found associations with prenatal exposure (Gladen et al., 2000).

Another longitudinal study that examined outcomes associated with lactational PCB exposures was a follow-up of 212 mother-infant pairs to determine whether earlier findings of adverse fetal and postnatal growth documented with prenatal exposures persisted through school age (Jacobson & Jacobson, 1996). Although prenatal exposure to PCBs was associated with significantly lower full-scale and verbal IQs, the authors did not find a relationship between exposure during breastfeeding and poorer cognitive performance on any of the three IQ and achievement tests used in their study.

Walkowiak and co-authors (2001) published their results of a cohort study conducted to determine whether the negative neurological effects of PCB exposure that had been documented earlier by other researchers (Winneke et al., 1998) resulted from pre- or postnatal exposure. In this case the investigators were able to demonstrate that PCB levels in breast milk may affect later development; overall postnatal exposure was related to lower Kaufman scores at 42 months of age. Consistent with earlier studies (Gladen et al., 1988; Koopman-Esseboom et al., 1996), however, they did not find any association between breast milk exposures and Bayley scores.

The most recent longitudinal study that analyzed breast milk exposures to PCBs and adverse outcomes in children involved a group of 182 children in the Faroe Islands (Grandjean et al., 2003). The aim of that study was to determine whether reduced growth of breastfed children was related to PCBs or methylmercury contaminants. They reported a decrease in both weight and height associated with doubling of PCB exposure at 42 months of age. The authors failed, however, to completely separate the impact of PCB breast milk exposures from prenatal exposures. In addition, the clinical significance of the deficits in weight and height (0.30 kg and 0.63 cm, respectively) was questionable (Jorissen, 2007).

Discussion and Recommendations

In summary, the clinical implications of risks associated with low-to-moderate PCB exposures via breastfeeding are not well established, and current evidence does not support advising mothers not to breastfeed their infants. Considerable variation in results across studies of PCB exposure and adverse fetal and childhood health effects (especially neurodevelopmental outcomes) exists. Longnecker and co-authors (2003) listed some of the factors that could be responsible for this variation, including protective influence of favorable child care settings in some groups; differences in PCB exposure levels (high, acute vs. low, chronic); differences in neurodevelopmental testing protocols; variation in the composition of the PCB mixtures across studies; and confounding by concurrent exposures such as mercury and omega-3 fatty acids.

The studies that examined the association between PCB lactational exposures and adverse health outcomes had significant limitations. Evidence for some associations came from examination of relatively small numbers of children with high-dose prenatal or early childhood exposures, such as offspring of women in the Yucheng and Yusho incidents. The majority of the studies were cross-sectional in design, and therefore unable to determine temporal patterns. Also, a lack of evidence exists regarding dose-response relationships of PCBs to toxicities discussed. Obvious ethical restrictions preclude the design of more robust research designs such as randomized trials.

Other reasons to support our recommendation of continuing to encourage maternal breastfeeding include the following: PCB analysis of breast milk is expensive, no defined normal values exist, and it is difficult to use the exposure information to predict individual health risks (Korrick & Altshul, 1998). In addition, standardized methods for exposure assessment are not available yet, especially among infants (Ayotte et al., 2003).

Two issues worth mentioning are the trends of reduced concentrations of PCBs and other persistent organohalogen residues and of an increase in the concentration of polybrominated diethers (PBDEs) in milk samples of mothers worldwide (Furst, 2006). PBDE concentrations in milk samples collected in the past five years are approximately 60% higher compared to specimens sampled 10 years before (She et al., 2007). PBDEs have now surpassed PCBs as a major environmental health concern in North America, and the absence of a positive correlation between PCBs and PBDE levels suggests differences may exist in exposure pathways for PBDEs and PCBs in humans (She et al., 2007). This worrisome trend warrants further investigation.

Maternal exposure to PCBs is predominantly through the food chain. Infant exposure to PCBs is predominantly through breastfeeding, although a significant contribution comes from transplacental passage. Research suggests that even the relatively smaller amounts of PCBs transferred in utero can affect the developing fetus (Jorissen, 2007) and should not be ignored. In fact, developmental deficits have been most consistently linked to prenatal, not postnatal, exposure to PCBs (Jacobson & Jacobson, 1996; Jacobson & Jacobson, 2001). Even at low concentrations, intrauterine exposures may be significant because of several factors: exposure is continuous; quantities transferred are substantial relative to the size of the developing fetus; and the fetus lacks the presence of protective barriers that are present postnatally (e.g., the blood brain barrier and fat deposits) that could cushion the detrimental effects of these agents (Jacobson et al., 1984). Fortunately, the beneficial effects of maternal breast milk can attenuate the adverse effect of both prenatal and postnatal exposures to PCBs (Boersma & Lanting, 2000). Therefore to lower PCB levels in childhood and reduce the potential adverse effects of PCB exposure, measures are needed that would affect both prenatal and postnatal risks of exposure to PCBs. The best approach is to educate future mothers to reduce their long-term dietary intake of PCBs before pregnancy in order to decrease the prospect of PCB transfer through both placental and lactational routes (Patan din et al., 1997).

In conclusion, despite the potential for PCB exposures via breast milk, limited evidence exists of significant toxicity associated with lactational transmission of these chemicals, especially at current background levels of environmental exposure. Breastfeeding should therefore continue to be encouraged on the basis of convincing evidence of the benefits derivable from human milk to the overall health and development of the infant.

Corresponding Author: Amina P. Alio, Research Assistant Professor, Department of Community and Family Health, College of Public Health, University of South Florida, 13201 Bruce B. Downs Blvd., MDC 56, Tampa, FL 33612. E-mail: aalio@health.usf.edu.

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Title Annotation:ADVANCEMENT OF THE SCIENCE
Author:Aliyu, Muktar H.; Alio, Amina P.; Salihu, Hamisu M.
Publication:Journal of Environmental Health
Article Type:Report
Geographic Code:1USA
Date:Oct 1, 2010
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