PCB concentration in the breast milk of Inuit mothers: Causes and impact on the development of newborns

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Introduction

PCBs, or polychlorinated biphenyls, are chemical compounds that now banned from production due to their harmful roles as organic pollutants[1]. However, PCBs are still persistent in the environment because of slow degradation processes, large scale accumulation, and illegal deposition of waste[2][1]. These factors lead to a gradual accumulation of toxic PCB compounds in the trophic food chain, which culminates to harmful levels in higher organisms, such as humans[2].

PCBs are suspected to have a variety of effects on the human body, including endocrine dysregulation and negative neurological effects[3][2][4]. Inuit populations are disproportionately found to have increased PCB concentrations due to their traditional diets that are likely to contain high levels of PCBs[3][5][6]. Environmental contaminants, such as PCBs, can travel through breast milk to infants. Children exposed to PCBs via diet have shown neurological and motor developmental problems[7].

The primary goal in helping to reduce the impacts of PCBs on public health and the environment is to prevent contamination. However, additional mechanisms must be in place to remediate the existing PCBs. These include but are not limited to: natural attenuation, physical and chemical methods, bioremediation through microbial applications or phytoremediation and more. Future directions for the remediation of PCBs will ideally work together to have a positive synergistic effect on the environment, as well as Inuit and global populations.

What are PCBs?

Structure

Examples of the diversity in PCB structure.

PCBs vary greatly in structure and in turn cause diverse toxic effects on humans and animals. They are chemically comprised of two phenyl groups that have at least two chloride side groups attached to the phenyls. In addition to their wide variety, their structure is relatively stable, allowing for their characteristic persistence as organic pollutants [8]. The metabolism of PCBs results in harmful byproducts or downstream metabolites that cause risk of oxidative stress and other health risks[9].

Origins

Printing inks are an example of commercialized items that were produced with PCBs prior to the 1970s.

PCBs were synthesized in high abundance, producing approximately 1.5 million tons from 1920 to 1980. Notable characteristics of PCBs include non-flammability, chemical stability, high boiling point and more which made them attractive compounds in industrial products[10]. These compounds were added abundantly into common products such as resins, rubber, inks and more. Once the toxic and persistent properties of PCBs was realized, the bioaccumulation of PCBs in landfills and the food chain had already begun. Regardless, a global ban was placed on these compounds in the late 1970s, however, these compounds continue to be found in air, soil, and sediment today. Upon ingestion of PCBs, they are able to accumulate in the adipocytes, or the fat cells, of the consumer. The presence of the PCBs in the fat cells allows for transfer via mammalian breast milk[8].

Risks

The effects of PCBs are commonly classified into two categories: dioxin-like and non-dioxin-like. Dioxin-like effects include the PCBs ability to interact with Ah receptors in the body, which can induce dermal lesions, weight loss, immunosuppression and more[11]. In contrast, non-dioxin-like effects occur if the compound does not interact with the Ah receptors and instead result in neurotoxicity, carcinogenicity and more[11].

The main source of exposure to PCBs occurs from ingesting PCB-contaminated foods[10]. An example of the effects of PCBs include adverse effects in a population exposed to A1221, a type of PCB. The population showed alteration of serum luteinizing hormone, an important hormone in reproductive regulation. Notably, the researchers found more significant alterations in the offspring of this population[10]. In addition to hormonal effects, dioxin-like PCBs can interact with Ah receptors and induce oxidative stress[8]. Other effects of PCBs include their carcinogenicity, environmental harm, and more.

Health Effects and Accumulation in Breast Milk

Human Health Effects

As PCB pollutants have persisted in the environment, their health effects on both humans and animals have been well studied. In humans, exposure via consumption of contaminated food sources like fish leads to acute and chronic health conditions. Among these conditions, hepatic, cardiovascular disorders, immune disorders, endocrine dysfunction, and reproductive issues are the most catastrophic[12]. The ingestion of PCBs can lead to these health issues by upregulating genes that promote inflammation and oxidative stress mechanisms, which in turn cause disease[13].

Bottom feeding large fish, like this striped bass, are most likely to contain high PCB concentrations.

Most low level exposures will not result in life threatening disease conditions. Studies done on animal exposure reveal that chronic low level PCB exposure can affect reproduction and fertility, the liver, immune system, and lead to body weight loss[14]. There is little available literature that analyzes the health effects of low level chronic PCB exposure in humans, but it is predicted that there will be similar effects as in the animal studies.

People with occupations in plants and factories that manufacture and handle products containing PCBs are the most at risk for chronic high levels of PCB exposure and the associated health risks[14]. The main health effects from occupational exposure that have been identified are liver damage, acne and dermal lesions, and respiratory issues[14].

Map representing an outline of Inuit peoples' land

Inuit populations, especially those in remote maritime communities, have been found to have significantly higher levels of blood PCBs than other Canadian populations due to a diet high in fish, beluga, seal, narwhal, and polar bears[15][16]. These animals have high fat content, where PCB is stored, and they lay at the top of their food web, resulting in high accumulation of PCBs. Studies have linked the high pollutant exposure seen exclusively in this population to health issues like chronic high cholesterol and heart disease[17]. It is also likely that the majority of Inuit people would experience the health effects associated with low level exposure.  

Pregnant People and Fetuses

A particularly detrimental health effect of PCB exposure is the potential to negatively impact pregnant populations and their fetuses. PCBs are known to cross the placenta and reach the fetus if the mother has been exposed to sufficiently high levels of PCBs, and they accumulate in the blood serum[18].

  • Pregnant people exposed to PCBs display similar health effects as the general population, however, they are considered an at risk population because they are more susceptible to disease development[14]. As such, many governments advise pregnant people against the consumption of fish from regions where PCB contamination is high[14]. Not only do PCBs negatively impact pregnant people, but PCB contamination carries a risk for fetal development pre and postnatal.
    A microscopy image of a sample of healthy human breast milk.
  • Fetuses can be exposed to PCBs through blood serum that crosses the placenta in utero and through breast milk to infants[19]. Since PCBs are lipid soluble, they are stored in adipose tissue in high concentrations. The lipids in this tissue are then mobilized to produce breast milk, transmitting PCBs along with other beneficial compounds[20]. This can affect the quality of the breast milk, resulting in a reduction of nutrients. Though PCBs and their metabolites pass to the infant in higher concentrations through breast milk, prenatal exposure through the placenta has more drastic health effects[21].
  • Inuit pregnant people, who have higher exposure to PCB contaminants are more likely to pass the pollutants on to their fetus in utero through the placenta, and postnatally through breast milk[16].  

Diagnosis/Detection

Depending on what doctors and researchers wish to study, blood samples are taken from pregnant people in the second or third trimester of their pregnancy. Blood samples can also be taken from the plasma post delivery and the fetus. All blood samples are centrifuged to glean plasma, which can then be analyzed for many PCB pollutants and their metabolites at an analytical laboratory[21].

Effects on Newborn Development

In addition to the well established negative impacts that PCBs have on adult health, neonatal exposure has been found to have a variety of detrimental neurological and developmental effects on infants and young children[22].

Neurological and Cognitive Impacts

PCB exposure has been linked to cognitive and behavioral delays in infants and children. According to cohort studies that focus on developmental neurotoxicity of PCBs, infants that have been exposed to high levels of PCBs in the womb or through breast milk have been correlated with lower IQ scores, reduced cognitive function, and behavioral problems such as hyperactivity, attention deficits, and impaired memory abilities[23]. A study on 5-year-old Inuit children found a small positive correlation between PCB levels at 2 months of age and inattention in childhood,  suggesting that early postnatal exposure can have negative behavioral impacts [24]. Interestingly, the authors also reason that the benefits of breastfeeding likely outweigh the risks of PCB exposure, encouraging Inuit families to not be deterred by the study’s findings.

The cerebellum is the brain region responsible for mediating fine motor skills. It is possible that this region is affected by PCBs during development.

The general consensus of historical research on infant health “demonstrated a correlation between perinatal exposure and poorer neurological development”[25]. One cohort study found that children who experienced high levels of post-natal PCB exposure in breast milk were also more likely to be in the lower range of average IQ scores and fall behind in reading comprehension.

Impacts on Motor Development

PCB exposure during infancy can also cause developmental delays in crucial areas such as motor skills. A cohort study in North Carolina found that post-natal exposure to PCBs via breast milk was correlated with lower scores on the psychomotor developmental index of the infants, although still within the normal range[25]. These results are notable since breastfeeding has been found to support infant development, yet this evidence suggests that PCB contamination appears to impede some benefits of breastmilk[25].

Postnatal exposure from other dietary sources can also have detrimental effects on children’s health, which mirror the motor delays correlated to post-natal exposure through breastmilk. A study done on eleven-year-old children subjected to seafood-based postnatal PCB exposure found, “PCB plasma concentrations were associated with poorer manual dexterity and slower fine motor speed”[22]. The results of the study found that fine motor speed is much more affected by postnatal exposure than prenatal exposure, corroborating the idea that postnatal exposure can have risks.

Remediation

To solve this problem, the primary goal is to stop contamination in the first place, which avoids any harmful effects on ecosystems and the people in them. However, once the contamination has occurred, there are several remediation techniques that have ben developed and used to either remove or neutralize the PCBs. These techniques can be in situ, where the treatment is performed directly at the site of contamination, or ex situ, where the contaminated materials (soil, sediment, etc.) are removed and treated off-site. Different remedial solutions have varying degrees of success and side effects, there is currently no ideal one-size-fits-all solution. The following are some common and well-researched techniques that have been used in the past or show promise for the future.

Natural attenuation

Dredging is one way to physically remove PCBs from sediment

Natural attenuation encompasses the in situ natural processes that result in remediation[26]. Some examples of natural attenuation include the transformation of PCBs into less harmful forms by microbial growth, or natural capping, which is the process in which clean new sediment settles on top of the contaminated one[27][26]. Both of these methods results in reduced bioavailability of the PCBs, mitigating the effects on the environment[26]. However, these natural processes do not always occur, and they do not solve the immediate negative effects of the PCB contamination. Additionally, they require long-term monitoring which is a financial burden. Generally, these methods are inefficient and additional human intervention is needed for bioremediation[26].

Physical methods

Some common physical methods of PCB remediation are ex situ, and used to treat contaminated materials like soil or sediment which have ben dug up and collected. "Dig and dump" is a straightforward solution of removing the polluted materials and leaving them in a landfill[26]. This solution merely removes the PCBs from one environment, but they still exist and may become environmental hazards in the future. Incineration of the PCB materials is a historical solution that is commonly used in areas of high pollution[27]. This treatment involves high temperatures and is effective at removing the compounds, but it may also result in other dangerous compounds forming as side effects[27]. These techniques are difficult to carry out if the polluted area is on a large scale, and are considered disruptive to the ecosystems[26].

Bacteria that grow on phenyls like this are often also able to grow on PCBs due to the similarity between their chemical structures

Chemical methods

Chemical remediation can take many forms, but the underlying technique is to use chemical processes to degrade or alter the structures of the PCBs to less harmful states[27]. Chemical reduction involves introducing metals in the environment which react with the PCBs and cause their dechlorination to an attenuated form which is more susceptible to degradation[27]. Chemical oxidation is similarly a method of adding reagents to the contaminated area to react and degrade the PCBs[27]. Chemical techniques are often highly effective and efficient, though these depend on the composition of the PCBs present[27][28]. One downside is that introducing chemicals in situ may negatively impact the ecosystems around, so care must be taken to choose appropriate reagents[27].

Bioremediation

Microbial remediation

Microbial degradation is the use of microbial metabolism to break down PCBs, often through anaerobic dechlorination or aerobic degradation[26]. Some bacteria are able to grow on phenyls like PCBs, so they produce dioxygenase enzymes which attack the PCBs and metabolize them to less harmful products like benzoic acid[29]. The benefits to microbial degradation are that the bacteria often do not disrupt the ecosystems, and the environmental footprint of this approach is generally low, as it takes advantage of natural biological processes[28]. However, the byproducts produced can still be harmful (albeit less so) and the time frame can vary with PCB variant and bacterial strain used[28]. The main factor that affects the efficacy and speed of the degradation is the bacterial strain used, as different strains have unique specificities for the chemical structure of the PCBs, so there is some optimization and troubleshooting involved in implementing this technique[28].

Some plant roots can extract PCBs from soil and uptake them into the plants

Phytoremediation

Phytoremediation is the uptake of PCBs through plants, resulting in their accumulation or degradation within the plants[30]. Additionally, the plant roots can enhance the soil environment for increased microbial activity to degrade PCBs[30]. The benefits of this remediation technique are the generally low environmental impacts on the soils, and the fact that plants can be genetically modified to be more efficient at uptake[30][28]. However, if the plants introduced are not native to the area, they may become an invasive species and harm the ecosystem[28]. As well, this method takes long-term monitoring and is dependent on the annual growth patterns of plants, so it is not very efficient and there can be inconsistency based on climate[28]. Finally, the plants are often unable to completely degrade the PCBs once they have been taken up, so there can be difficulties with separating the PCBs from the biomass[30].

Other

Other remediation methods to treat PCB contamination in the environment can vary from thermal treatments to immobilize pollutants and make them easier to extract, or using activated carbon to bind and contain the PCBs[26][31]. The combination of multiple techniques is also possible, and can have synergistic effects[26]. For example, activated carbon is often used to accumulate PCBs to improve the efficacy of microbial remediation by concentrating the pollutants[28]. By combining remediation techniques, PCB clean-up can be optimized to reduce environmental disruption while maximizing effectiveness.

Conclusion

High levels of polychlorinated biphenyls (PCBs) in the environment is a concerning conservation and human health issue that disproportionately affects Inuit populations, especially Inuit mothers and their children. Due to mass production of PCB containing products in the mid 1900s, PCBs persist as pollutants in a vast majority of environments and accumulate in fat deposits of the food chain, resulting in concentrated PCB levels in higher trophic groups[4][8]. Because humans generally lie at the top of the food chain, when ingested, PCBs are found in elevated concentrations within the lipophilic components of the body. Such high PCB levels have been identified to cause a multitude of chronic health effects[9].

Inuit communities are especially vulnerable to PCB exposure due to their traditional diet of marine mammals, which are high in fat and can store increased levels of lipophilic environmental contaminants[5]. Due to the natural strains of pregnancy, Inuit mothers have increased risks associated with PCB contamination. Furthermore, PCBs can pass from mothers into fetuses and infants through placental blood and breast milk[7]. In Inuit communities, pre and neonatal exposure has been linked with neurological, motor skill, and cognitive developmental impacts[21][22][25].

Since the contaminant persists in the environment, the majority of efforts to decrease human health impacts consist of remediation techniques that remove or inactivate PCBs. These techniques range from physical methods, like dig and dump, to bioremediation that uses natural methods to metabolize or sequester PCBs[26][27]. While a variety of methods exist to remove PCBs from the environment, there is currently no solution that eliminates the health and environmental threat of PCBs without the introduction of other issues. Depending on the environmental situation, a combination of one or more techniques presents the best solution to limit PCB exposure. Further research is required in order to maximize the effectiveness of remediation methods, without introducing new environmental disruptions.

Bibliography

  1. ↑ 1.0 1.1 Liu, Jing; Tan, Ya; Song, Erqun; Song, Yang (July 2017). "A Critical Review of Polychlorinated Biphenyls Metabolism, Metabolites, and Their Correlation with Oxidative Stress". Chemical Research in Toxicology. 33 (8): 2022–2042.
  2. ↑ 2.0 2.1 2.2 La Rocca, Cinzia; Mantovani, Alberto (2006). "From environment to food: the case of PCB". Annali dell'Istituto superiore di sanita. 42 (4): 410–416.
  3. ↑ 3.0 3.1 Dallaire, R. (2009). "Thyroid hormone levels of pregnant inuit women and their infants exposed to environmental contaminants". Environmental health perspectives. 117(6): 1014–1020.
  4. ↑ 4.0 4.1 Cinzia, La Rocca; Mantovani, Alberto (2006). "From environment to food: the case of PCB". Annali dell'Istituto superiore di sanita. 42 (4): 410–416.
  5. ↑ 5.0 5.1 Adamou, Thérèse Yéro; Riva, Mylène; Muckle, Gina; Sidi, Elhadji Anassour Laouan; Lemire, Mélanie; Ayotte, Pierre (2020). "Blood mercury and plasma polychlorinated biphenyls concentrations in pregnant Inuit women from Nunavik: Temporal trends". The Science of the Total Environment. 743.
  6. ↑ Verner, M. A. (2015). "Prenatal and early-life polychlorinated biphenyl (PCB) levels and behavior in Inuit preschoolers". Environment international. 78: 90–94.
  7. ↑ 7.0 7.1 American Academy of Pediatrics Committee on Drugs (2001). "The Transfer of Drugs and Other Chemicals Into Human Milk". Pediatrics. 108 (3): 776–789.
  8. ↑ 8.0 8.1 8.2 8.3 Liu, Jing; Tan, Ya; Song, Erqun; Song, Yang (July 2017). "A Critical Review of Polychlorinated Biphenyls Metabolism, Metabolites, and Their Correlation with Oxidative Stress". Chemical Research in Toxicology. 33 (8): 2022–2042.
  9. ↑ 9.0 9.1 Grimm, Fabian; Hu, Dingfei; Kania-Korwel, Izabela; Lehmler, Hans-Joachin; Ludewig, Gabriele; Hornbuckle, Keri; Duffel, Michael; Bergman, Åke; Robertson, Larry (2015). [10.3109/10408444.2014.999365 "Metabolism and metabolites of polychlorinated biphenyls"] Check |url= value (help). Critical Reviews in Toxicology. 45 (3): 245–272.
  10. ↑ 10.0 10.1 10.2 Faroon, Obaid; Ruiz, Patricia (July 2016). "Polychlorinated biphenyls: New evidence from the last decade". Toxicology and Industrial Health. 32 (11).
  11. ↑ 11.0 11.1 Giesy, John; Kannan, Kurunthachalam (January 1998). "Dioxin-Like and Non-Dioxin-Like Toxic Effects of Polychlorinated Biphenyls (PCBs): Implications For Risk Assessment". Critical reviews in toxicology. 28 (6): 511–569.
  12. ↑ Gupta, Prachi (2018). "The Environmental Pollutant, Polychlorinated Biphenyls, and Cardiovascular Disease: a Potential Target for Antioxidant Nanotherapeutics". Drug Delivery and Translation Research. 8.
  13. ↑ Liu, J (2020). "A Critical Review of Polychlorinated Biphenyls Metabolism, Metabolites, and Their Correlation with Oxidative Stress". Chemical Research in Toxicology. 33: 2022–2042.
  14. ↑ 14.0 14.1 14.2 14.3 14.4 Agency for Toxic Substances and Disease Registry (2014). "Polychlorinated Biphenyls Toxicity". Environmental Health and Medicine Education. Retrieved 9 April, 2023. Check date values in: |access-date= (help)
  15. ↑ Dewailly, E. (1994). "Exposure of remote maritime populations to coplanar PCBs". Environmental Health Perspectives. 102: 205–209.
  16. ↑ 16.0 16.1 Ayotte, P. (1997). "PCBs and dioxin-like compounds in plasma of adult Inuit living in Nunavik (Arctic Quebec)". Chemosphere. 34: 1459–1468 – via PubMed.
  17. ↑ Singh, Kavita (2018). "Association of blood polychlorinated biphenyls and cholesterol levels among Canadian Inuit". Environmental Research. 160: 298–305 – via Elsevier Science Direct.
  18. ↑ Popp, W. (1993). "[Polychlorinated biphenyls (PCBs) and reproduction disturbances]". Zentralblatt Fur Hygiene Und Umweltmedizin = International Journal of Hygiene and Environmental Medicine. 193: 528–556 – via PubMed.
  19. ↑ Park, June-Soo (2008). "Placental Transfer of Polychlorinated Biphenyls, Their Hydroxylated Metabolites and Pentachlorophenol in Pregnant Women from Eastern Slovakia". Chemosphere. 60: 1676–1684 – via PubMed.
  20. ↑ Mead, Nathaniel (2008). "Contaminants in Human Milk: Weighing the Risks against the Benefits of Breastfeeding". Environmental Health Perspectives. 116: 426–434 – via PubMed.
  21. ↑ 21.0 21.1 21.2 Soechitram, Shalini (2004). "Fetal Exposure to PCBs and Their Hydroxylated Metabolites in a Dutch Cohort". Environmental Health Perspectives. 112: 1208–1212.
  22. ↑ 22.0 22.1 22.2 Boucher, Olivier (2016, August 27). "Altered fine motor function at school age in Inuit children exposed to PCBS, methylmercury, and lead". Environment International. Check date values in: |date= (help)
  23. ↑ Dallaire, R. (2009). "Thyroid hormone levels of pregnant inuit women and their infants exposed to environmental contaminants". Environmental health perspectives. 117(6): 1014–1020.
  24. ↑ Verner, M. A. (2015). "Prenatal and early-life polychlorinated biphenyl (PCB) levels and behavior in Inuit preschoolers". Environment international. 78: 90–94.
  25. ↑ 25.0 25.1 25.2 25.3 Jorrissen, J. (2007). "Literature review. Outcomes associated with postnatal exposure to polychlorinated biphenyls (PCBs) via breast milk". Advances in neonatal care : official journal of the National Association of Neonatal Nurses. 7(5): 230–237.
  26. ↑ 26.0 26.1 26.2 26.3 26.4 26.5 26.6 26.7 26.8 26.9 Gomes, Helena I.; Dias-Ferreira, Celia; Ribeiro, Alexandra B. (2013). "Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for full-scale application". Science of The Total Environment. 445–446: 237–260.
  27. ↑ 27.0 27.1 27.2 27.3 27.4 27.5 27.6 27.7 27.8 Šrédlová, Kamila; Cajthaml, Tomáš (2022). "Recent advances in PCB removal from historically contaminated environmental matrices". Chemosphere. 287, Part 1: 132096.
  28. ↑ 28.0 28.1 28.2 28.3 28.4 28.5 28.6 28.7 Jing, Ran; Fusi, Soliver; Kjellerup, Birthe V. (2018). "Remediation of Polychlorinated Biphenyls (PCBs) in Contaminated Soils and Sediment: State of Knowledge and Perspectives". Frontiers in Environmental Science. 6.
  29. ↑ Furukawa, Kensuke; Fujihara, Hidehiko (2008). "Microbial degradation of polychlorinated biphenyls: Biochemical and molecular features". Journal of Bioscience and Bioengineering. 105 (5): 433–449.
  30. ↑ 30.0 30.1 30.2 30.3 Gomes, Helena I.; Dias-Ferreira, Celia; Ribeiro, Alexandra B. (2013). "Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for full-scale application". Science of The Total Environment. 445–446: 237–260.
  31. ↑ Lofrano, G; Libralato, G; Minetto, D; De Gisi, S; Todaro, F; Conte, B; Calabrò, D; Quatraro, L; Notarnicola, M (2017). "In situ remediation of contaminated marine sediment: an overview". Environmental science and pollution research international. 24 (6): 5189–5206.
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