Abstract
Objective
This study assessed the associations between blood levels of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and polychlorinated biphenyls (PCBs) and humoral and cellmediated immune response.
Methods
The subjects included 53 male workers who had worked at industrial waste incinerators for more than one year. The experimental groups were divided into indoor, field, and incinerator workers according to working process. Data on their lifestyles and occupational characteristics were collected using a survey, and blood levels of PCDDs, PCDFs, and PCBs were analyzed to determine their associations with T-lymphocyte subpopulations and immunoglobulin levels.
Results
The results showed that total blood dioxins PCB levels were higher in field and incinerator workers (20.46±22.21 and 21.97±18.05 pg toxic equivalence [TEQ]/g fat, respectively) than in indoor workers (7.69± 2.05 pg TEQ/g fat). CD3+, CD4+, CD8+, and CD4+ CD45RO+ cells among T-lymphocyte subpopulations and IgE and IgM levels among immunoglobulins were slightly higher in field and incinerator workers than those in indoor workers, with no statistical significance (p<0.05). Multiple linear regression analysis with Tlymphocyte subpopulations and immunoglobulins as dependent variables and PCDDS, PCDFs, and PCBs as independent variables showed that PCBs were negatively associated with CD3+ levels (B value=-56.890, 95% confidence interval [CI]=-104.39→ -9.392, p< 0.05) and were positively associated with the CD4+/CD8+ ratio (B value=0.149, 95% CI=0.001-0.297, p<0.05). In addition, PCB levels were associated with IgE (B value=248.703, 95% CI=153.79-343.62, p< 0.01), IgG (B value=52.078, 95% CI=0.344-103.812, p<0.05) and IgM levels (B value=53.153, 95% CI= 32.087-74.219, p<0.01).
Conclusion
These findings was obtained from a small number of subjects; hence, further studies including more subjects are necessary to validate the associations between blood levels of PCDDs, PCDFs, and PCBs and immune function.
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References
Whittaker, A., BeruBe, K., Jones, T., Maynard, R. & Richards, R. Killer smog of London, 50 years on: particle properties and oxidative capacity. Sci. Total Environ. 334, 435–445 (2004).
WHO. Preventing disease through healthy environments, http://apps.who.int/iris/bitstream/10665/204585/1/9789241565196_eng.pdf (2016).
Qing, X., Yutong, Z. & Shenggao, L. Assessment heavy metal pollution and human health risk in urban soils of steel industrial city (Anshan), Liaoning, Northeast China. Ecotoxicol. Environ. Saf. 120, 377–385 (2015).
Lu, Y., Song, S., Wang, R., Liu, Z. & Meng, J. Impacts of soil and water pollution on food safety and health risks in China. Environ. Int. 77, 5–15 (2015).
Weisglas-Kuperus, N. Neurodevelopmental, immunological and endocrinological indices of perinatal human exposure to PCBs and dioxins. Chemosphere 37, 1845–1853 (1998).
Startin, J. R. & Rose, M. D. in Dioxins and dioxin-like PCBs in food (eds Schecter, A. & Gasiewicz, T. A.) 89–136 (Wiley-Interscience, USA, 2003).
Wehrmeier, A., Lenoir, D., Schramm, K.-W., Zimmermann, R. & Haha, K. Patterns of isomers of chlorinated dibenzo-ρ-dioxins as tool for elucidation of thermal formation mechanisms. Chemosphere 36, 2775–2801 (1998).
Matsmoto, R., Tu, N. P. C., Haruta, S., Kawano, M. & Takeuchi, I. Analysis of all 209 polychlorinated biphenyl (PCB) congeners (with special reference to dioxinlike PCB congeners) in Japanese seabass and related species by high-resolution gas chromatography/highresolution mass spectrometry (HRGC/HRMS). Region. Studies Marine Sci. 3, 119–130 (2016).
Brouwer, A., Ahlborg, U. G., van den Berg, M., Birnbaum, L. S. & Boersma, E. R. Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants. Eur. J. Pharmacol. 293, 1–40 (1995).
Autrup, H. Ambient air pollution and adverse health effects. Procedia Soc. Behav. Sci. 2, 7333–7338 (2010).
Banerjee, M. et al. Hematological, immunological, and cardiovascular changes in individuals residing in a polluted city of India: A study in Delhi. Int. J. Hyg. Environ. Health 215, 306–311 (2012).
Kim, S.-A., Kim, K.-S., Lee, Y.-M., Jacobs, D. R. & Lee, D.-H. Associations of organochlorine pesticides and polychlorinated biphenyls with total, cardiovascular, and cancer mortality in elders with differing fat mass. Environ. Res. 138, 1–7 (2015).
Karras, J. G. & Holsapple, M. P. Inhibition of calcium-dependent B cell activation by 2,3,7,8-tetrachlorodibenzo-ρ-dioxin. Toxicol. Appl. Pharmacol. 125, 264–270 (1994).
Kimata, H. 2,3,7,8-Tetrachlorodibenzo-ρ-dioxin selectively enhances spontaneous IgE production in B cells from atopic patients. Int. J. Hyg. Environ. Health 206, 601–604 (2003).
Miyashita, C. et al. Effects of prenatal exposure to dioxin-like compounds on allergies and infections during infancy. Environ. Res. 111, 551–558 (2011).
Shepherd, D. M., Dearstyne, E. A. & Kerkvliet, N. L. The effects of TCDD on the activation of ovalbuminspecific DO11.10 transgenic CD4+ T cells in adoptively transferred mice. Toxicol. Sci. 56, 340–350 (2000).
Nohara, K. et al. Effects of 2,3,7,8-tetrachlorodibenzo-ρ-dioxins (TCDD) on T-cell-derived cytokine production in ovalbumin-immunized C57B1/6 mice. Toxicology 172, 49–58 (2002).
Inadera, H. The immune system as a target for environmental chemicals: Xenoestrogens and other compounds. Toxicol. Lett. 164, 191–206 (2006).
Schulz, V. J. et al. Activation of the aryl hydrocarbon receptor reduces the number of precursor and effector T cells, but preserves thymic CD4+CD25+Foxp3+ regulatory T cells. Toxicol. Lett. 215, 100–109 (2012).
Yamamoto, K., Kudo, M., Arito, H., Ogawa, Y. & Takata, T. Isomer pattern and elimination of dioxins in workers exposed at a municipal waste incineration plant. Ind. Health 53, 454–464 (2015).
Kim, K.-W., Park, S. H., Won, Y. L. & Lee, S. K. Effects of low-level exposure to manganese and lead on immune function. Anal. Sci. Technol. 27, 248–253 (2014).
Stanmore, B. R. The formation of dioxins in combustion system. Combust. Flame 136, 398–427 (2004).
Zhang, M., Buekens, A. & Li, X. Brominated flame retardants and the formation of dioxins and furans in fires and combustion. J. Hazard. Mater. 304, 26–39 (2016).
IARC. IARC monograph on the evaluation of carcinogenic risks to humans: Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans, http://monographs.iarc.fr/ENG/Monographs/vol69/mono69. pdf (1997).
Niittynen, M., Simanainen, U., Syrjala, P., Pohjanvirta, R. & Viluksela, M. Differences in acute toxicity syndromes of 2,3,7,8-tetrachlorodibenzo-p-dioxin and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin in rats. Toxicology 235, 39–51 (2007).
Ritz, S. A. Air pollution as a potential contributor to the ‘epidemic’ of autoimmune disease. Med. Hypotheses 74, 110–117 (2010).
Sorg, O. AhR signaling and dioxin toxicity. Toxicol. Lett. 230, 225–233 (2014).
Poiger, H. & Schlatter, C. Pharmacokinetics of 2,3,7,8-TCDD in man. Chemosphere 15, 1489–1494 (1986).
Milbrath, M. O. et al. Apparent half-lives of dioxins, furans and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ. Health Perspect. 117, 417–425 (2009).
Park, H., Park, E. & Chang, Y.-S. Ten-year time trend of dioxins in human serum obtained from metropolitan populations in Seoul, Korea. Sci. Total Environ. 470-471, 1338–1345 (2014).
Muto, H. & Takizawa, Y. Dioxins in cigarette smoke. Arch. Environ. Health 44, 171–174 (1989).
Uehara, R., Nakamura, Y., Matsuura, N., Kondo, N. & Tada, H. Dioxins in human milk and smoking of mothers. Chemosphere 68, 915–920 (2007).
Rogan, W. J. et al. Polychlorinated biphenyls (PCBs) and dichlorodiphenyl dichloroethan (DDE) in human milk: effects of maternal factors and previous lactation. Am. J. Public Health 76, 172–177 (1986).
Pluim, H. J., Kramer, I., van der Slikke, J. W., Koppe, J. G. & Olie, K. Levels of PCDDs and PCDFs in human milk: dependence on several parameters and dietary habits. Chemosphere 26, 1889–1895 (1993).
Kvalem, H. E., Brantsæter, A. L., Meltzer, H. M., Stigum, H. & Thomsen, C. Development and validation of prediction models for blood concentrations of dioxins and PCBs using dietary intakes. Environ. Int. 50, 15–21 (2012).
Shin, E.-S., Kim, J., Choi, S.-D., Kang, Y.-W. & Chang, Y.-S. Estimated dietary intake and risk assessment of polychlorinated dibenzo-ρ-dioxins and dibenzofurans and dioxin-like polychlorinated biphenyls from fish consumption in the Korean general population. Chemosphere 146, 419–425 (2016).
Michot, J. M. et al. Immune-related adverse events with immune chechpoint blockade: a comprehensive review. Eropean J. Cancer 54, 139–148 (2016).
Jang, S. H., Choi, Y.-J. & Kim, K.-W. Influence of chronic low-level exposure to toluene on cell-mediated immunity. J. Korean Soc. Occup. Environ. Hygiene 23, 266–272 (2013).
Kim, K.-W., Park, S. H. & Won, Y. L. Effects of low-level exposure to manganese and lead on immune function. Anal. Sci. Technol. 27, 248–253 (2014).
Nagayama, J. et al. Effects of contamination level of dioxins and related chemicals on thyroid hormone and immune response systems in patients with “Yusho”. Chemosphere 43, 1005–1010 (2001).
Uchi, H., Yasukawa, F. & Furue, M. Prevalence of atopic dermatitis and serum IgE of Yusho patients born before 1967. Fukuoka Igku Zasshi 102, 100–104 (2011).
Budnik, L. T., Wegner, R., Rogall, U. & Baur, X. Accidental exposure to polychlorinated biphenyls (PCBs) in waste cargo after heavy seas. Global waste transport as a source of PCBs exposure. Int. Arch. Occup. Environ. Health 87, 125–135 (2014).
Sulentic, C. E. W., Holsapple, M. P. & Kaminski, N. E. A putative link between transcriptional regulation of IgM expression by 2,3,7,8-tetrachlordibenzo-p-dioxin and the AhR/DRE signaling pathway. J. Pharmacol. Exp. Ther. 295, 705–716 (2000).
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Kim, KW., Won, Y.L. & Ogawa, Y. Associations between Blood Levels of Polychlorinated Dibenzo-p-dioxins/Furans and Polychlorinated Biphenyls with Immune Systems. Toxicol. Environ. Health Sci. 10, 17–25 (2018). https://doi.org/10.1007/s13530-018-0342-8
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DOI: https://doi.org/10.1007/s13530-018-0342-8