Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Dietary Habits and Cooking Methods Could Reduce Avoidable Exposure to PCBs in Maternal and Cord Sera

Abstract

Polychlorinated biphenyls (PCBs), like other persistent organic pollutants, are accumulating throughout the food chain and pose health threats to humans, especially children and foetuses. There is no protocol for reducing the contamination levels of the PCBs in humans. This study identified food items and cooking methods that reduce serum PCB levels by analysing data collected from the Chiba Study of Mother and Child Health. The sample size was 194 subjects. Serum PCB levels were measured using gas chromatography–electron capture negative ionization quadrupole mass spectrometry. Information on dietary habits was obtained from a brief diet history questionnaire that included questions about food items and cooking methods. Food items were categorized into food groups, and nutrient levels were calculated based on food item consumption. Principal component analysis and lasso regression were used as statistical methods. The analyses of food items and nutrients suggested that food items rich in dietary fibre reduce avoidable exposure to PCBs, as could grilling and deep frying of food, which could reduce avoidable exposure to serum PCBs in mothers and foetuses. (174 words).

Introduction

Previous studies have shown that virtually every person on this planet has been exposed to persistent organic pollutants (POPs) via different intermediaries (e.g., air, water, and food)1,2,3,4. POPs tend to accumulate in the fatty tissues of our bodies because of their high chemical stability, persistence, and pronounced lipophilicity. These factors make it difficult to reduce contamination levels5,6,7. The health threats posed by POPs to humans have been investigated in several cohort studies worldwide8,9,10,11,12. These studies have revealed that exposure to one of the more common types of POP, polychlorinated biphenyls (PCBs), increases the risk of cancer13,14,15 and causes liver dysfunction, skin lesions (chloracne), and nervous system abnormalities8. PCBs also affect the immune system16,17 and increase mortality rates from cardiovascular disease9. Foetuses and children are more susceptible to these environmental contaminants than adults1. Studies show that children exposed to PCBs experience poor cognitive function in early childhood10,11,18. Furthermore, exposure to high levels of PCBs during the foetal period leads to a low birth weight in infants19,20,21,22. Therefore, reducing the contamination level of PCBs in humans could significantly improve the health of future generations.

The food chain is the primary source of POP bioaccumulation5. Previous studies have shown that fish and meat (e.g., beef, pork, and chicken) are the main food sources of POP exposure (e.g., PCBs)23,24,25, despite the essential nutrients provided by these foods26. It has also been shown that the contamination levels of POPs differ in different food items23,27,28. Furthermore, cooking methods may reduce PCB levels in different food items29,30.

Previous studies have tested various interventions to reduce PCB levels in humans, such as drug treatment and dietary methods. Studies have indicated that drugs such as colestimide reduce blood dioxin levels (i.e., polychloro-dibenzon-p-dioxin, polychloro-dibenzofuran, and coplanar polychlorinated benzene)31,32. However, colestimide produces numerous side effects (e.g., gastrointestinal bleeding and vitamin and calcium deficiency). A recent study also showed that colestimide may not effectively reduce serum PCB levels in Yusho patients (people who were exposed to rice oil contaminated with PCBs and dioxin-like compounds in 1968)33. Attempts have also been made to reduce the contamination levels of POPs through dietary methods. Fermented brown rice with Aspergillus oryzae 34 and dietary olestra34 may reduce PCB levels in the body. Additionally, cooking processes can reduce the concentration of organic environmental pollutants (e.g., PCBs) in food items29,30. Nevertheless, appropriate guidelines for reducing POP contamination in humans have yet to be established, despite the efforts made in these studies.

The present study examined the relationship between dietary habits, based on a comparatively low-cost data transfer method involving a brief diet history questionnaire (BDHQ), and serum PCB levels in maternal and cord blood from pregnant women in Japan according to the measures proposed in a recent report35. The data analysed in this study were obtained from the Chiba Study of Mother and Child Health (C-MACH)36, which is a birth cohort study based on the developmental origins of health and disease hypothesis, performed in pregnant women who enrolled at less than 13 weeks of gestation. We analysed the relationship between serum PCB levels and food groups (following37). We then investigated the relationship between serum PCB levels and different nutrients, calculated based on the consumption of food items. We also examined the association between serum PCB levels and different cooking methods. This study determined an effective intervention method for reducing serum PCB levels.

Materials and Methods

Set-up

Dietary data from the BDHQ and data on serum PCB levels were obtained from the Onodera Ladies Clinic and Yamaguchi Women’s Hospital in Japan. The recruitment period was February 2014 to June 2015. The participants in this study were pregnant women at <13 weeks of gestation and their unborn children. We will continue with follow-up surveys until the children reach 5 years of age. The data used in this study were collected during the last trimester of pregnancy. Stillbirths and data from mother and child pairs or children of women who withdrew their consent were excluded, as were data from women who transferred to another hospital during the data collection period. The Biomedical Research Ethics Committee of the Graduate School of Medicine of Chiba University approved this study (ID: 759), which was performed in accordance with the approved guidelines and regulations of the Declaration of Helsinki. Written informed consent was obtained from each participant.

A total of 289 samples were initially collected from the Onodera Ladies Clinic and Yamaguchi Women’s Hospital. Some samples were removed because key information was missing (i.e., the mother’s body mass index (BMI), age, parity, BDHQ, or PCB levels in maternal serum), which reduced the sample size to 202. The sample size was further reduced to 194 after excluding mothers who consumed alcohol during pregnancy. The final analysed sample size for investigating the association of PCB levels in maternal and cord serum with dietary habits and cooking methods was 189 after the removal of samples with missing data on PCB levels in cord serum.

Data acquisition

The mothers’ age and parity were obtained from the questionnaires at 12 weeks of gestation, and their BMIs were calculated based on the physical information acquired from the questionnaires. The mothers’ dietary habits were recorded using the BDHQ during the last trimester, including information about both food items and cooking methods. The contamination levels of serum PCBs were assessed in maternal blood samples collected at an average of 35 weeks of gestation, with a range of 30 to 39 weeks of gestation (Onodera Ladies Clinic: average: 32 weeks of gestation, range: 30 to 36 weeks of gestation; Yamaguchi Women’s Hospital: average: 36 weeks of gestation, range: 34 to 39 weeks of gestation) and cord blood. PCB levels in the serum samples from maternal and cord blood were analysed using gas chromatography–electron capture negative ionization quadrupole mass spectrometry (GC-NICI-qMS)38.

The serum samples (0.3–0.4 g) were desaturated using 1 M potassium hydroxide/MeOH (1 mL) in the GC-NICI-qMS analysis. Target compounds were extracted twice with n-hexane (500 μL), and the samples were spiked with PCB 23, 30, 55, and 207 (40 pg each) as surrogate internal standards. The two extracts were combined and washed with ultrapure water. The remaining residue after evaporation of the solvent was dissolved in n-hexane (3 mL), passed through a glass column packed with 44% sulfuric acid silica gel (500 mg), and concentrated until almost dry. PBB 154 (20 pg) dissolved in decane (200 μL) was added as a syringe spike.

The instrument used for the analyses was a JMS-Q1050GC (JEOL Ltd., Tokyo, Japan) quadrupole mass spectrometer equipped with an Agilent 7890B gas chromatograph and a 7693 autosampler (Agilent Technologies Inc., Tokyo, Japan). An HP5-MSUI fused-silica capillary column (30 m × 0.25 mm ID × 0.25 μm film Agilent Technologies Inc., Tokyo, Japan) was employed for GC separation. The injector was operated in pulsed splitless mode at 280 °C. Helium (Purity: >99.99995) was used as the GC carrier gas at a constant flow rate of 1.3 mL/min, and methane (Purity: >99.999) was the reagent gas for the NICI source. The identification and quantification of the 24 PCB congeners were achieved via monitoring of chlorine ions [Cl: m/z: 35] through selected ion monitoring (SIM) analysis using a NICI-MS detector.

The samples employed in this study were QA/AC samples collected from a PCB measurement campaign of performed in our laboratory36, which is accredited in compliance with ISO/IEC 17025:2005 standards (Accreditation of Certification Body: Japan Accreditation Board). The detection limits for individual PCBs using this method were 1.9–20 pg g−1 wet wt. An inter-calibration exercise organized by the NIST using Standard Reference Material 195739 was applied to ensure the quality and analyses of PCBs.

Statistical analysis

Dietary data were re-sorted into food groups based on a previous study prior to the primary analysis37. This organization reduced the number of parameters in the analysis. The nutrient contents of the food items were calculated based on the consumption amounts indicated in the BDHQ, to further investigate the association between serum PCB levels and dietary habits40.

The main analysis tool used in this study was R ver. 3.3.341. A principal component analysis (PCA) using the FactoMineR package42 was combined with lasso regression43 to analyse the relationship between serum PCB levels and different food groups. The lasso regression was used to analyse the relationship between serum PCB levels and nutrients and that between serum PCB levels and cooking methods. Some of the mothers’ characteristics (e.g., parity, BMI, and age)44 were also included in the analyses of the relationships between dietary habits and serum PCB levels because of the high correlation between serum PCB levels and these indices.

Results

Participant characteristics

Table 1 presents the maternal demographics and lifestyle characteristics employed for the analyses in this study (n = 194), including age, BMI, parity, marital status, infertility treatment, smoking history, and education. Table 1 shows that 93.81% of the participants were over 25 years old and that 75.26% had a BMI between 18.5 and 24.9. Most of the participants (98.97%) were married; 80.41% exhibited an education level above high school; and 80.93% were non-smokers. Additionally, 89.18% of the participants had received no infertility treatment, and 40.21% of the participants were nulliparous.

Table 1 Maternal characteristics in the analysed sample.

Analyses of PCB levels

Table 2 provides a summary of the analyses of PCB levels in maternal and cord sera. PCB concentrations in cord serum were highly correlated with those in maternal serum. Twenty-four PCB congeners were identified in this study; CB28, CB60, CB66, CB87, CB178, CB199, CB206, and CB209 were omitted from the summary (Table 2) because of a low detection rate in the samples (less than 50% in maternal serum and less than 25% in cord serum). The median concentrations of total PCBs in the maternal and cord sera were 0.37 and 0.10 ng g−1 wet wt., respectively. The maximum concentration of total PCBs in maternal and cord sera were 1.48 and 0.51 ng g−1 wet wt., respectively. The dominant congeners of the PCBs in the maternal and cord blood sera were CB138, CB153, and CB180, which is consistent with the results of previous studies45,46,47,48,49,50,51,52,53. The concentration of PCBs detected in the blood in this study was lower than in previous studies45,46,47,51,53,54,55. The reason for this difference may be that the subjects of this study were young perinatal women, in whom serum PCB concentrations either may be low due to their young age or may be lowered as a result of pregnancy56.

Table 2 Distribution of PCB congeners in maternal and cord sera (LOD: limit of detection).

PCA of the different congeners of PCBs measured in maternal and cord sera was also performed (Fig. 1). CB99, CB105, CB126, CB177, and CB183 were further excluded from the analyses of PCBs in cord serum because of their low concentrations (median < limitation of detection) (Table 2). The results show that the dispersion of different congeners of PCBs was low (aligned in the same direction of PC1) in maternal and cord blood sera. Therefore, we used the total PCBs for the main analysis in this study.

Figure 1
figure 1

PCA for various PCB congeners measured in maternal blood during the last trimester and cord blood (PC1 vs. PC2). Sixteen PCB congeners (CB74, CB99, CB105, CB118, CB126, CB138, CB146, CB153, CB156, CB170, CB177, CB180, CB183, CB187, CB194, and CB201) are shown for maternal blood; eleven PCB congeners (CB74, CB118, CB138, CB146, CB153, CB156, CB170, CB180, CB187, CB194, CB201) are shown for cord blood.

Main results

Table 3 presents the results of the association analysis between maternal serum PCB levels and the consumed food groups, analysed using the combination of PCA and lasso regression. Parity was negatively related to PCB levels in maternal and cord sera, and the mother’s BMI and age showed a positive relation, which corresponds to previous studies44,57,58,59. The top three explained variant components (PC1, PC2, and PC3) were positively related to PCB levels in maternal and cord sera. Comparison of the association between each principal component and PCB levels in maternal serum revealed that the association was weaker in cord serum.

Table 3 Combination of PCA and lasso regression for food groups and PCB levels in maternal and cord sera (adjusted by parity, mothers’ BMI, and mothers’ age).

Figures 2 and 3 illustrate the correlations between different food groups and the relationship between serum PCB levels and food groups (PC1 vs. PC2 and PC1 vs. PC3, respectively). Figure 2 shows that fish/shellfish, seaweed, mushrooms, and vegetables (Group 1) were correlated with each other, as were meat, potatoes, eggs, and dairy products (Group 2). Group 3 included cola, juice, noodles, and confectionery. There also appeared to be a correlation between fruits, pickled vegetables, green tea, black tea, coffee, and bread (Group 4). Rice was on the opposite side of Group 4. Figure 3 shows the correlation between fish/shellfish, green and yellow vegetables, other vegetables (not including green and yellow vegetables), seaweed, and pulses (Group 5). Confectionery, coffee, juice, and cola appeared on the opposite side of Group 5. Meat, pickled vegetables, potatoes, and fruits (Group 6) exhibited a correlation, with noodles on the opposite side. Rice, green tea, and black tea (Group 7) also appeared to correlate with each other, and bread was on the opposite side of Group 7.

Figure 2
figure 2

PCA for different food groups and serum PCB levels (PC1 vs. PC2). Twenty-two food groups (dairy, meat, fish and shellfish, eggs, pulses, potatoes, pickled vegetables, green and yellow vegetables, other vegetables, mushroom, seaweed, confectioneries, fruits, oils, bread, noodles, green tea, black tea, coffee, coke, juice, sugar, and rice) are shown.

Figure 3
figure 3

PCA for different food groups and serum PCB levels (PC1 vs. PC3). Twenty-two food groups (dairy, meat, fish and shellfish, eggs, pulses, potatoes, pickled vegetables, green and yellow vegetables, other vegetables, mushroom, seaweed, confectioneries, fruits, oils, bread, noodles, green tea, black tea, coffee, coke, juice, sugar, and rice) are shown.

The results for PC1 indicated that foods in Group 1 and Group 2 positively contributed to the elevation of serum PCB levels, and foods in Group 3 presented a negative contribution. The results for PC2 suggested that rice positively contributed to the elevation of serum PCB levels, and foods in Group 4 made a negative contribution. The results for PC3 revealed that foods in Group 6 (dairy products and bread) made a positive contribution to the elevation of serum PCB levels, and foods in Group 7 (vegetables other than green and yellow vegetables, seaweed, and pulses) made a negative contribution. These correlations between different food items suggest that vegetables, fruits, mushrooms, rice, tea, seaweed, and pulses, which contain a comparatively high amount of dietary fibre, are negatively associated with an increase in serum PCB levels.

A lasso regression was performed to investigate the association between nutrients and PCB levels in maternal and cord sera (Table 4). The regression showed that most of the nutrients were excluded from the analyses of PCB levels in maternal serum because of a low correlation. The nutrients that exhibited a comparatively strong negative association with serum PCB levels included manganese, pantothenic acid, saturated fatty acid, and total dietary fibre. However, the difference in the distribution of manganese, pantothenic acid, and saturated fatty acid between different food items was quite small, and the amount of dietary fibre was high in food items such as vegetables, tea, rice, and pulses60. A similar observation was made in the analysis of the association between nutrients and PCB levels in cord serum.

Table 4 Lasso regression for nutrients and PCB levels in maternal and cord sera (adjusted by parity, mothers’ BMI, and mothers’ age).

We further analysed the relationship between cooking methods and PCB levels in maternal and cord sera using lasso regression (Table 5). The results revealed that grilling of fish and meat was negatively associated with serum PCB levels. Deep frying of food items other than fish was also negatively associated with serum PCB levels. Grilled meat exerted a greater negative effect on serum PCB levels than grilled and deep-fried fish. The association between PCB levels in cord sera and cooking methods was weaker overall than that for maternal sera because of the low PCB concentration in cord sera.

Table 5 Lasso regression of cooking methods and PCB levels in maternal and cord sera (adjusted by parity, mothers’ BMI, and mothers’ age).

Discussion

Dietary habits are closely associated with the contamination levels of PCBs in humans because exposure to PCBs primarily occurs via the food chain4,5, and some food items and cooking processes reduce avoidable exposure to PCBs (Figs 2 and 3, and Table 5). Therefore, we investigated the relationship between PCB contamination levels and different dietary habits and cooking methods. The results presented in Figs 2 and 3 suggested that people who consumed fish, meat, and vegetables tended to eat less junk food. People who frequently consumed junk food tended to eat bread as a staple food rather than rice. Overall, the results show that people who ate regular meals (e.g., consumed foods such as fish, meat, vegetables, rice, and bread) tended to exhibit comparatively high contamination levels of PCBs. This tendency occurred because food items such as fish, meat, eggs, and dairy products are the main food sources of PCB exposure23,24,25,27,61,62. However, the results also indicated that foods such as vegetables, fruits, mushrooms, rice, tea, seaweed, and pulses reduced avoidable exposure to PCBs in maternal and cord sera. Analyses of the associations between nutrients and serum PCB levels revealed that nutrients were distributed comparatively equally among different food items, and dietary fibre reduced avoidable exposure to PCBs. High contents of dietary fibre are found in food items such as vegetables, fruits, seaweed, rice, nuts, pulses, and tea60, which is consistent with the results shown in Figs 2 and 3. Therefore, the consumption of food items that contain a high content of dietary fibre may reduce avoidable exposure to PCBs, as suggested in previous studies63,64,65,66,67.

Previous studies have suggested that cooking reduces PCB levels in food26,68, and the reduction of PCB contamination by cooking depends on the particular food item and the applied cooking method. A general reduction of fatty tissue in food items may decrease the contamination levels of PCBs because of the lipophilic properties of PCBs29,30. The present study showed that grilling and deep frying were associated with lower serum levels of PCBs. Grilling reduces the contamination level of PCBs due to the loss of fatty tissue during the cooking process, and deep frying extracts PCBs into the cooking oil. However, grilling fish was not as effective as grilling meat in lowering serum levels of PCBs because of the comparatively high concentration of PCBs in fish15 (Table 5). Previous studies have indicated that deep frying is the most effective cooking method for reducing PCB levels in food69, but we found that deep frying was not as effective as grilling. We may have obtained this result because of the particular cooking methods used by the participants in this study. For example, grilling was employed to cook fish and meat, and deep frying was used to cook meat and vegetables. Therefore, the effect of PCB reduction on vegetables could have been low because the contamination level in vegetables was low27. Another reason may be the changes in the texture of the food associated with different cooking methods. For example, any burnt areas on food may obstruct the absorption of PCBs during digestion.

Other studies have also shown that the concentration of PCBs is correlated with the concentration of other POPs, such as organohalogen pesticides, polybrominated diphenyl ethers, PCDDs, and PCDFs28,54. Reduction interventions to avoid PCB exposure may also be used for these POPs because most of these POPs exhibit lipophilic properties similar to PCBs. The analysis of serum PCB levels revealed that the correlation between maternal serum PCB levels and cord serum PCB levels was high (Table 2). PCB contamination in cord serum is related to the health of the foetus. Therefore, a lower maternal level of PCBs may reduce PCB contamination levels in foetuses. However, the data employed in this study were acquired from pregnant women in Japan, and dietary habits are likely different in other countries. People in countries and regions near the sea, such as Japan, tend to consume more fish than meat. However, people living in inland countries and regions tend to consume more meat. Therefore, the results may differ if the analysed data were to be collected from an inland country or region. Different dietary habits in different countries and regions should be considered in future studies.

This study has some limitations. First, the sample size was comparatively small (n = 194). Therefore, a cohort study with a larger sample size should be performed in the future. Second, crossover analyses involving the consumption of different food items and use of different cooking methods were not performed in this study. A case-control study of this nature based on human subjects may result in an even smaller sample size and increase the likelihood of bias. Furthermore, a case-control study with animals may not reflect the situation in humans because of the differences in human and animal metabolism. Finally, the data on cooking methods obtained from the BDHQ were not comprehensive. For example, deep frying applied to meat and vegetables. Thus, a more detailed questionnaire design is required for further studies.

In conclusion, we investigated the relationship between serum PCB levels and dietary habits in pregnant Japanese women by analysing food items, nutrients, and cooking methods using a BDHQ. The results of the analyses of food items and nutrients suggest that food items such as vegetables, fruits, mushrooms, rice, seaweed, pulses, nuts, and tea, which are rich in dietary fibre, are associated with lower serum levels of PCBs. The results also revealed that cooking methods, such as grilling and deep frying, were associated with lower serum levels of PCBs. However, further investigation must be performed to verify the effects of dietary fibre and cooking methods based on case-control studies, to establish a protocol for healthy dietary habits. The health of future generations may be improved if guidelines for healthy dietary habits are introduced for pregnant women and children from a young age.

References

  1. Mori, C. & Todaka, E. Environmental Contaminants and Children’s Health: Sustainable Health Science for Future Generations. (MARUZEN PLANET Co., Ltd. at https://books.google.co.jp/books?id=O28PjwEACAAJ, 2011).

  2. Covaci, A., Tutudaki, M., Tsatsakis, A. M. & Schepens, P. Hair analysis: Another approach for the assessment of human exposure to selected persistent organochlorine pollutants. Chemosphere 46, 413–418 (2002).

    ADS  CAS  Article  PubMed  Google Scholar 

  3. Wilhelm, M., Ewers, U. & Schulz, C. Revised and new reference values for some trace elements in blood and urine for human biomonitoring in environmental medicine. Int. J. Hyg. Environ. Health 207, 69–73 (2004).

    CAS  Article  PubMed  Google Scholar 

  4. Sharma, B. M. et al. Environment and human exposure to persistent organic pollutants (POPs) in India: A systematic review of recent and historical data. Environ. Int. 66, 48–64 (2014).

    CAS  Article  PubMed  Google Scholar 

  5. Armitage, J. M. & Gobas, F. A. P. C. A terrestrial food-chain bioaccumulation model for POPs. Environ. Sci. Technol. 41, 4019–4025 (2007).

    ADS  CAS  Article  PubMed  Google Scholar 

  6. Fujii, S., Polprasert, C., Tanaka, S., Lien, N. P. H. & Qiu, Y. New POPs in the water environment: Distribution, bioaccumulation and treatment of perfluorinated compounds - A review paper. J. Water Supply Res. Technol. - AQUA 56, 313–326 (2007).

    CAS  Article  Google Scholar 

  7. Gobas, F. A. P. C., de Wolf, W., Burkhard, L. P., Verbruggen, E. & Plotzke, K. Revisiting bioaccumulation criteria for POPs and PBT assessments. Integr. Environ. Assess. Manag. 5, 624–637 (2009).

    CAS  Article  PubMed  Google Scholar 

  8. Longnecker, Matthew, P., Rogan, Walter, J. & Lucier, G. The human health effects of DDT (dichlorobiphenyl-trichloroethane) and PCBs (polychlorinated biphenyls) and an overview of organochlorines in public health. Ann Rev Public Heal. 18, 211–244 (1997).

    CAS  Article  Google Scholar 

  9. Gustavsson, P. & Hogstedt, C. A cohort study of Swedish capacitor manufacturing workers exposed to polychlorinated biphenyls (PCBs). Am. J. Ind. Med. 32, 234–239 (1997).

    CAS  Article  PubMed  Google Scholar 

  10. Schantz, S. L., Widholm, J. J. & Rice, D. C. Effects of PCB exposure on neuropsychological function in children. Environ. Health Perspect. 111, 357–376 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Ayotte, P., Muckle, G., Jacobson, J. L., Jacobson, S. W. & Dewailly, É. Assessment of pre- and postnatal exposure to polychlorinated biphenyls: Lessons from The Inuit Cohort Study. Environ. Health Perspect. 111, 1253–1258 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Ross, G. The public health implications of polychlorinated biphenyls (PCBs) in the environment. Ecotoxicol. Environ. Saf. 59, 275–291 (2004).

    CAS  Article  PubMed  Google Scholar 

  13. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Polychlorinated Biphenyls, in ‘IARC Monographs on the Evaluation of Carcinogenic Risks to Humans’. 107 (2015).

  14. Pohl, H. et al. Toxicological profile for chlorinated dibenzo-p-dioxins. Agency Toxic Subst. Dis. Regist. 1–532, https://doi.org/10.1201/9781420061888_ch51 (1998).

  15. Giesy, J. P. & Kannan, K. Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): Implications for risk assessment. Crit. Rev. Toxicol. 28, 511–569 (1998).

    CAS  Article  PubMed  Google Scholar 

  16. Ansar Ahmed, S. The immune system as a potential target for environmental estrogens (endocrine disrupters): A new emerging field. Toxicology 150, 191–206 (2000).

    CAS  Article  Google Scholar 

  17. Lee, D. H., Steffes, M. & Jacobs, D. R. Positive associations of serum concentration of polychlorinated biphenyls or organochlorine pesticides with self-reported arthritis, especially rheumatoid type, in women. Environ. Health Perspect. 115, 883–888 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Jacobson, J. L. & Jacobson, S. W. Methodological issues in research on developmental exposure to neurotoxic agents. Neurotoxicol. Teratol. 27, 395–406 (2005).

    CAS  Article  PubMed  Google Scholar 

  19. Eguchi, A., Sakurai, K., Watanabe, M. & Mori, C. Exploration of potential biomarkers and related biological pathways for PCB exposure in maternal and cord serum: A pilot birth cohort study in Chiba, Japan. Environ. Int. 102, 157–164 (2017).

    CAS  Article  PubMed  Google Scholar 

  20. Karmaus, W. & Zhu, X. Maternal concentration of polychlorinated biphenyls and dichlorodiphenyl dichlorethylene and birth weight in Michigan fish eaters: a cohort study. Environ. Heal. 3, 1 (2004).

    Article  Google Scholar 

  21. Weight, B. et al. Review and Dichlorodiphenyldichloroethylene (DDE): A Meta-analysis within 12 European Birth Cohorts 162, 162–170 (2012).

  22. Baibergenova, A., Kudyakov, R., Zdeb, M. & Carpenter, D. O. Low birth weight and residential proximity to PCB-contaminated waste sites. Environ. Health Perspect. 111, 1352–1357 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Domingo, J. L. & Bocio, A. Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: A literature review. Environ. Int. 33, 397–405 (2007).

    CAS  Article  PubMed  Google Scholar 

  24. Smith, A. G. & Gangolli, S. D. Organochlorine chemicals in seafood: Occurrence and health concerns. Food Chem. Toxicol. 40, 767–779 (2002).

    CAS  Article  PubMed  Google Scholar 

  25. Larsen, J. C. Risk assessments of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and dioxin-like polychlorinated biphenyls in food. Mol. Nutr. Food Res. 50, 885–896 (2006).

    CAS  Article  PubMed  Google Scholar 

  26. Rimm, E. B. Fish Intake. Contaminants, and Human Health. 296, 1885–1900 (2015).

    Google Scholar 

  27. Törnkvist, A., Glynn, A., Aune, M., Darnerud, P. O. & Ankarberg, E. H. PCDD/F, PCB, PBDE, HBCD and chlorinated pesticides in a Swedish market basket from 2005 - Levels and dietary intake estimations. Chemosphere 83, 193–199 (2011).

    ADS  Article  PubMed  Google Scholar 

  28. Sasamoto, T. et al. Estimation of 1999-2004 dietary daily intake of PCDDs, PCDFs and dioxin-like PCBs by a total diet study in metropolitan Tokyo, Japan. Chemosphere 64, 634–641 (2006).

    ADS  CAS  Article  PubMed  Google Scholar 

  29. Perelló, G., Martí-Cid, R., Castell, V., Llobet, J. M. & Domingo, J. L. Influence of various cooking processes on the concentrations of PCDD/PCDFs, PCBs and PCDEs in foods. Food Control 21, 178–185 (2010).

    Article  Google Scholar 

  30. Domingo, J. L. Influence of Cooking Processes on the Concentrations of Toxic Metals and Various Organic Environmental Pollutants in Food: A Review of the Published Literature. Crit. Rev. Food Sci. Nutr. 51, 29–37 (2010).

    Article  Google Scholar 

  31. Sakurai, K., Todaka, E., Saito, Y. & Mori, C. Pilot study to reduce dioxins in the human body. Intern. Med. 43, 792–5 (2004).

    CAS  Article  PubMed  Google Scholar 

  32. Sakurai, K. et al. Colestimide Reduces Blood Polychlorinated Biphenyl (PCB) Levels. Intern. Med. 45, 327–328 (2006).

    Article  PubMed  Google Scholar 

  33. Todaka, T. et al. Effect of colestimide on the concentrations of polychlorinated dibenzo-p-dioxins, polychlorinated dizenzofurans, and polychlorinated biphenyls in blood of Yusho patients. Environ. Heal. 15, 63 (2016).

    Article  Google Scholar 

  34. Jandacek, R. J. et al. Reduction of the body burden of PCBs and DDE by dietary intervention in a randomized trial. J. Nutr. Biochem. 25, 483–488 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Mori, C. & Todaka, E. For a healthier future: a virtuous cycle for reducing exposure to persistent organic pollutants. J. Epidemiol. Community Health jech-2016–208088, https://doi.org/10.1136/jech-2016-208088 (2017).

  36. Sakurai, K. et al. Chiba study of Mother and Children’s Health (C-MACH): cohort study with omics analyses. BMJ Open 6, e010531 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kobayashi, S. et al. Comparison of relative validity of food group intakes estimated by comprehensive and brief-type self-administered diet history questionnaires against 16 d dietary records in Japanese adults. Public Health Nutr. 14, 1200–1211 (2011).

    Article  PubMed  Google Scholar 

  38. Eguchi, A., Enomoto, T., Suzuki, N., Okuno, M. & Mori, C. Development of Simple Analytical Methods of Polychlorinated Biphenyls in Human Serum by Gas Chromatography Negative Ion Chemical Ionization Quadrupole Mass Spectrometry. Acta Chromatogr. 1–4, https://doi.org/10.1556/1326.2017.00029 (2017).

  39. Page, S. R. M. S. July 2009 NIST SRM 1957 Organic Contaminants in Non-Fortified Human Serum NIST SRM 1958 Organic Contaminants in Fortified Human Serum SRM Spotlight NIST SRM 2855 Additive Elements in Polyethylene. 3–4 (2009).

  40. Sasaki, S., Yanagibori, R. & Amano, K. Self-administered diet history questionnaire developed for health education: a relative validation of the test-version by comparison with 3-day diet record in women. J. Epidemiol. 8, 203–215 (1998).

    CAS  Article  PubMed  Google Scholar 

  41. R Development Core Team. R: A Language and Environment for Statistical Computing, 3-900051-07-0 (2017).

  42. Husson, A. F., Josse, J., Le, S., Mazet, J. & Husson, M. F. Package ‘ FactoMineR’, https://doi.org/10.1007/978-3-540-74686-7 (2014).

  43. Friedman, A. J., Hastie, T., Tibshirani, R. & Hastie, M. T. Package ‘ glmnet’ (2013).

  44. Hardell, E., Carlberg, M., Nordström, M. & van Bavel, B. Time trends of persistent organic pollutants in Sweden during 1993-2007 and relation to age, gender, body mass index, breast-feeding and parity. Sci. Total Environ. 408, 4412–4419 (2010).

    ADS  CAS  Article  PubMed  Google Scholar 

  45. Park, J. S. et al. Polychlorinated biphenyls and their hydroxylated metabolites (OH-PCBs) in pregnant women from eastern Slovakia. Environ. Health Perspect. 115, 20–27 (2007).

    CAS  Article  PubMed  Google Scholar 

  46. Park, J. S. et al. Placental transfer of polychlorinated biphenyls, their hydroxylated metabolites and pentachlorophenol in pregnant women from eastern Slovakia. Chemosphere 70, 1676–1684 (2008).

    ADS  CAS  Article  PubMed  Google Scholar 

  47. Fängström, B., Athanasiadou, M., Grandjean, P., Weihe, P. & Bergman, Å. Hydroxylated PCB metabolites and PCBs in serum from pregnant faroese women. Environ. Health Perspect. 110, 895–899 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Glynn, A. et al. Determinants of serum concentrations of organochlorine compounds in Swedish pregnant women: a cross-sectional study. Environ. Heal. 6, 2 (2007).

    Article  Google Scholar 

  49. Bradman, A. et al. Polybrominated diphenyl ether levels in the blood of pregnant women living in an agricultural community in California. Environ. Health Perspect. 115, 71–74 (2007).

    CAS  Article  PubMed  Google Scholar 

  50. Berglund, M. et al. Inter-individual variations of human mercury exposure biomarkers: a cross-sectional assessment. Environ. Heal. A Glob. Access Sci. Source 4, 20 (2005).

    Google Scholar 

  51. Wittsiepe, J. et al. PCDD/F and dioxin-like PCB in human blood and milk from German mothers. Chemosphere 67 (2007).

  52. Huisman, M. et al. Perinatal exposure to polychlorinated biphenyls and dioxins through dietary intake. Chemosphere 31, 4273–87 (1995).

    ADS  CAS  Article  PubMed  Google Scholar 

  53. Bjerregaard, P. & Hansen, J. C. Organochlorines and heavy metals in pregnant women from the Disko Bay area in Greenland. Sci. Total Environ. 245, 195–202 (2000).

    ADS  CAS  Article  PubMed  Google Scholar 

  54. Ochiai, S. et al. A pilot study for foetal exposure to multiple persistent organic pollutants and the development of infant atopic dermatitis in modern Japanese society. Chemosphere 94, 48–52 (2014).

    ADS  CAS  Article  PubMed  Google Scholar 

  55. Wolff, M. S., Deych, E., Ojo, F. & Berkowitz, G. S. Predictors of organochlorines in New York City pregnant women, 1998-2001. Environ. Res. 97, 170–177 (2005).

    CAS  Article  PubMed  Google Scholar 

  56. Mori, C. et al. Polychlorinated biphenyl levels in the blood of Japanese individuals ranging from infants to over 80 years of age. Environ. Sci. Pollut. Res. 21, 6434–6439 (2014).

    CAS  Article  Google Scholar 

  57. Nichols, B. R., Hentz, K. L., Aylward, L., Hays, S. M. & Lamb, J. C. Age-specific reference ranges for polychlorinated biphenyls (PCB) based on the NHANES 2001-2002 survey. J. Toxicol. Environ. Health. A 70, 1873–7 (2007).

    CAS  Article  PubMed  Google Scholar 

  58. Voorspoels, S., Covaci, A., Maervoet, J. & Schepens, P. Relationship between age and levels of organochlorine contaminants in human serum of a Belgian population. Bull. Environ. Contam. Toxicol. 69, 22–29 (2002).

    CAS  Article  PubMed  Google Scholar 

  59. Černá, M. et al. Serum concentrations of indicator PCB congeners in the Czech adult population. Chemosphere 72, 1124–1131 (2008).

    ADS  Article  PubMed  Google Scholar 

  60. Kagawa, A. Kagawa Nutrition University Publishing Division Food Composition Table 2014 - Reference material. (Kagawa Nutrition University Publishing Division, 2014).

  61. Darnerud, P. O. et al. Dietary intake estimations of organohalogen contaminants (dioxins, PCB, PBDE and chlorinated pesticides, e.g. DDT) based on Swedish market basket data. Food Chem. Toxicol. 44, 1597–1606 (2006).

    CAS  Article  PubMed  Google Scholar 

  62. Harrison, N. et al. Time trends in human dietary exposure to PCDDs, PCDFs and PCBs in the UK. Chemosphere 37, 1657–1670 (1998).

    ADS  CAS  Article  PubMed  Google Scholar 

  63. Morita, K., Hamamura, K. & Lida, T. Binding of PCB by Several Types of Dietary Fiber in vivo and in vitro. Fukuoka Igaku Zasshi 212–217 (1995).

  64. Iida, T. et al. Clinical trial of a combination of rice bran fiber and cholestyramine for promotion of fecal excretion of retained polychlorinated dibenzofuran and polychlorinated biphenyl in Yu-Cheng patients. Fukuoka Igaku Zasshi 86, 226–33 (1995).

    CAS  PubMed  Google Scholar 

  65. Junya Nagayama et al. Promotive Excretion of Causative Agents of Yusho by Fermented Brown Rice with Aspergillus oryze in Yusho Patients. Fukuoka Igaku Zasshi 123–129 (2011).

  66. Morita, K., Matsueda, T. & Iida, T. Effect of dietary fiber on fecal excretion and liver distribution of PCDF in rats. Fukuoka Igaku Zasshi 86, 218–225 (1995).

    CAS  PubMed  Google Scholar 

  67. Nagayama, J., Takasuga, T., Tsuji, H. & Iwasaki, T. Promotive excretion of causative agents of Yusho by one year intake of FBRA in Japanese people. Fukuoka Igaku Zasshi 96, 241–248 (2005).

    CAS  PubMed  Google Scholar 

  68. Tsutsumi, T. et al. Recent survey and effects of cooking processes on levels of PCDDs, PCDFs and Co-PCBs in leafy vegetables in Japan. Chemosphere 46, 1443–1449 (2002).

    ADS  CAS  Article  PubMed  Google Scholar 

  69. Moya, J., Garrahan, K. G., Poston, T. M. & Durell, G. S. Effects of cooking on levels of PCBs in the fillets of winter flounder. Bull. Environ. Contam. Toxicol. 60, 845–851 (1998).

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the Environmental Research and Technology Development Fund (funding number: 5-1652) of the Ministry of the Environment of Japan. Funding was also received from a Grant-in-Aid for Scientific Research (A) (grant number: 16H01781) from the Japan Society for the Promotion of Science. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the anonymous reviewers whose comments and suggestions helped us improve this manuscript. We also appreciate all the participants in this study and the staff who helped us with data collection and measurements. We thank Katie Stallard, LLB, from the Edanz Group (www.edanzediting.com/ac) and Nature Research Editing Service Team for editing a draft of this manuscript.

Author information

Authors and Affiliations

Authors

Contributions

C.M., A.E. and M.O. conceived and designed the study. M.W. and H.N. collected and processed the data. A.E. performed the measurement of PCBs. W.J. analysed the data and wrote the manuscript. C.M., E.T., A.E. and K.S. supervised the research and revised the manuscript. All authors reviewed the manuscript.

Corresponding author

Correspondence to Chisato Mori.

Ethics declarations

Competing Interests

The authors declare that they have no competing interests.

Additional information

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jin, W., Otake, M., Eguchi, A. et al. Dietary Habits and Cooking Methods Could Reduce Avoidable Exposure to PCBs in Maternal and Cord Sera. Sci Rep 7, 17357 (2017). https://doi.org/10.1038/s41598-017-17656-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-017-17656-9

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing