Association between blood levels of PCDDs/PCDFs/dioxin-like PCBs and history of allergic and other diseases in the Japanese population

  • Mariko Nakamoto
  • Kokichi Arisawa
  • Hirokazu Uemura
  • Sakurako Katsuura
  • Hidenobu Takami
  • Fusakazu Sawachika
  • Miwa Yamaguchi
  • Tomoya Juta
  • Tohru Sakai
  • Eisaku Toda
  • Kei Mori
  • Manabu Hasegawa
  • Masaharu Tanto
  • Masayuki Shima
  • Yoshio Sumiyoshi
  • Kenji Morinaga
  • Kazunori Kodama
  • Takaichiro Suzuki
  • Masaki Nagai
  • Hiroshi Satoh
Original Article

Abstract

Background

Previous studies reported that exposure to dioxins was associated with an increased risk of various diseases in general populations.

Objectives

The aim of this study was to examine the association between levels of dioxins in blood and allergic and other diseases.

Methods

We conducted a cross-sectional study on 1,063 men and 1,201 women (aged 15–76 years), who were living throughout Japan and not occupationally exposed to dioxins, during 2002–2010. In fasting blood samples, polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and dioxin-like PCBs (DL-PCBs) were analyzed by isotope dilution high-resolution gas chromatography/mass spectrometry. We obtained information on life style and self-reported history of diseases using a questionnaire. Blood pressure, blood levels of hemoglobin A1c, and serum lipids were also measured. Multiple logistic regression models were used to analyze the association between dioxin levels in blood and various diseases.

Results

Toxic equivalents of PCDDs/PCDFs and total dioxins showed significant inverse dose–response relationships with atopic dermatitis, after adjustments for potential confounders. The highest quartile for total dioxins had an adjusted odds ratio of 0.26 (95 % confidence interval 0.08–0.70) compared to the reference group (first quartile). The odds ratios for hypertension, diabetes mellitus, hyperlipidemia, gout in men, and gynecologic diseases in women significantly increased with increasing toxic equivalents of PCDDs/PCDFs, DL-PCBs, and total dioxins in blood.

Conclusions

The present findings suggest that background exposure to dioxins was associated with reduced risk of atopic dermatitis. The results also support the idea that low-level exposure to dioxins is associated with an increased risk of diabetes, hypertension, and hyperlipidemia.

Keywords

Allergic diseases Atopic dermatitis DL-PCBs PCDDs PCDFs Gout 

References

  1. Arisawa K, Matsumura T, Tohyama C, Saito H, Satoh H, Nagai M, Morita M, Suzuki T (2003) Fish intake, plasma omega-3 polyunsaturated fatty acids, and polychlorinated dibenzo-p-dioxins/polychlorinated dibenzo-furans and co-planar polychlorinated biphenyls in the blood of the Japanese population. Int Arch Occup Environ Health 76:205–215Google Scholar
  2. Arisawa K, Takeda H, Mikasa H (2005) Background exposure to PCDDs/PCDFs/PCBs and its potential health effects: a review of epidemiologic studies. J Med Invest 52:10–21CrossRefGoogle Scholar
  3. Biedermann T, Röcken M (1999) Th1/Th2 balance in atopy. Springer Semin Immunopathol 21:295–316CrossRefGoogle Scholar
  4. Calvert GM, Willie KK, Sweeney MH, Fingerhut MA, Halperin WE (1996) Evaluation of serum lipid concentrations among US workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Arch Environ Health 51:100–107CrossRefGoogle Scholar
  5. Choi HK, Atkinson K, Karlson EW, Willett W, Curhan G (2004) Purine-rich foods, dairy and protein intake, and the risk of gout in men. N Engl J Med 350:1093–1103CrossRefGoogle Scholar
  6. Eskenazi B, Mocarelli P, Warner M, Samuels S, Vercellini P, Olive D, Needham LL, Patterson DG Jr, Brambilla P, Gavoni N, Casalini S, Panazza S, Turner W, Gerthoux PM (2002) Serum dioxin concentrations and endometriosis: a cohort study in Seveso, Italy. Environ Health Perspect 110:629–634CrossRefGoogle Scholar
  7. Everett CJ, Frithsen IL, Diaz VA, Koopman RJ, Simpson WM Jr, Mainous AG III (2007) Association of a polychlorinated dibenzo-p-dioxin, a polychlorinated biphenyl, and DDT with diabetes in the 1999–2002 national health and nutrition examination survey. Environ Res 103:413–418CrossRefGoogle Scholar
  8. Fromme H, Albrecht M, Boehmer S, Büchner K, Mayer R, Liebl B, Wittsiepe J, Bolte G (2009) Intake and body burden of dioxin-like compounds in Germany: the INES study. Chemosphere 76:1457–1463CrossRefGoogle Scholar
  9. Fujimaki H, Nohara K, Kobayashi T, Suzuki K, Eguchi-Kasai K, Tsukumo S, Kijima M, Tohyama C (2002) Effect of a single oral dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin on immune function in male NC/Nga mice. Toxicol Sci 66:117–124CrossRefGoogle Scholar
  10. Ha MH, Lee DH, Son HK, Park SK, Jacobs DR Jr (2009) Association between serum concentrations of persistent organic pollutants and prevalence of newly diagnosed hypertension: results from the national health and nutrition examination survey 1999–2002. J Hum Hypertens 23:274–286CrossRefGoogle Scholar
  11. Henriksen GL, Ketchum NS, Michalek JE, Swaby JA (1997) Serum dioxin and diabetes mellitus in veterans of operation ranch hand. Epidemiology 8:252–258CrossRefGoogle Scholar
  12. Hirota Y, Kataoka K, Tokunaga S, Hirohata T, Shinohara S, Tokiwa H (1993) Association between blood polychlorinated biphenyl concentration and serum triglyceride level in chronic “Yusho” (polychlorinated biphenyl poisoning) patients. Int Arch Occup Environ Health 65:221–225CrossRefGoogle Scholar
  13. Hsu JF, Lee CC, Su HJ, Chen HL, Yang SY, Liao PC (2009) Evaluation of background persistent organic pollutant levels in human from Taiwan: polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls. Environ Int 35:33–42CrossRefGoogle Scholar
  14. Ito T, Inouye K, Nohara K, Tohyama C, Fujimaki H (2008) TCDD exposure exacerbates atopic dermatitis-related inflammation in NC/Nga mice. Toxicol Lett 177:31–37CrossRefGoogle Scholar
  15. Kremmyda LS, Vlachava M, Noakes PS, Diaper ND, Miles EA, Calder PC (2011) Atopy risk in infants and children in relation to early exposure to fish, oily fish, or long-chain omega-3 fatty acids: a systematic review. Crit Rev Allergy Immunol 41:36–66CrossRefGoogle Scholar
  16. Laughter D, Istvan JA, Tofte SJ, Hanifin JM (2000) The prevalence of atopic dermatitis in Oregon schoolchildren. J Am Acad Dermatol 43:649–655CrossRefGoogle Scholar
  17. Lee DH, Lee IK, Song K, Steffes M, Toscano W, Baker BA, Jacobs DR Jr (2006) A strong dose-response relation between serum concentrations of persistent organic pollutants and diabetes: results from the National Health and Examination Survey 1999–2002. Diabetes Care 29:1638–1644CrossRefGoogle Scholar
  18. Lee DH, Lee IK, Porta M, Steffes M, Jacobs DR Jr (2007) Relationship between serum concentrations of persistent organic pollutants and the prevalence of metabolic syndrome among non-diabetic adults: results from the national health and nutrition examination survey 1999–2002. Diabetologia 50:1841–1851CrossRefGoogle Scholar
  19. Lindström G, Hooper K, Petreas M, Stephens R, Gilman A (1995) Workshop on perinatal exposure to dioxin-like compounds. V. Summary. Environ Health Perspect 103:135–142Google Scholar
  20. Lorber M, Patterson D, Huwe J, Kahn H (2009) Evaluation of background exposures of Americans to dioxin-like compounds in the 1990s and the 2000s. Chemosphere 77:640–651CrossRefGoogle Scholar
  21. Luebke RW, Copeland CB, Daniels M, Lambert AL, Gilmour MI (2001) Suppression of allergic immune responses to house dust mite (HDM) in rats exposed to 2,3,7,8-TCDD. Toxicol Sci 62:71–79CrossRefGoogle Scholar
  22. Miyashita C, Sasaki S, Saijo Y, Washino N, Okada E, Kobayashi S, Konishi K, Kajiwara J, Todaka T, Kishi R (2011) Effects of prenatal exposure to dioxin-like compounds on allergies and infections during infancy. Environ Res 111:51–58CrossRefGoogle Scholar
  23. Nakamura T, Nakai K, Matsumura T, Suzuki S, Saito Y, Satoh H (2008) Determination of dioxins and polychlorinated biphenyls in breast milk, maternal blood and cord blood from residents of Tohoku, Japan. Sci Total Environ 394:39–51CrossRefGoogle Scholar
  24. Ngoc PL, Gold DR, Tzianabos AO, Weiss ST, Celedon JC (2005) Cytokines, allergy, and asthma. Curr Opin Allergy Clin Immunol 2:161–166CrossRefGoogle Scholar
  25. Palomares O, Yaman G, Azkur AK, Akkoc T, Akdis M, Akdis CA (2010) Role of Treg in immune regulation of allergic diseases. Eur J Immunol 40:1232–1240CrossRefGoogle Scholar
  26. Park H, Kang JH, Baek SY, Chang YS (2010) Relative importance of polychlorinated naphthalenes compared to dioxins, and polychlorinated biphenyls in human serum from Korea: contribution to TEQs and potential sources. Environ Pollut 158:1420–1427CrossRefGoogle Scholar
  27. Porpora MG, Medda E, Abballe A, Bolli S, De Angelis I, di Domenico A, Ferro A, Ingelido AM, Maggi A, Panici PB, De Felip E (2009) Endometriosis and organochlorinated environmental pollutants: a case-control study on Italian women of reproductive age. Environ Health Perspect 117:1070–1075Google Scholar
  28. SAS Institute (1997) SAS/STAT software: changes and enhancements through release 6.12. SAS Institute, CaryGoogle Scholar
  29. Sasamoto T, Ushio F, Kikutani N, Saitoh Y, Yamaki Y, Hashimoto T, Horii S, Nakagawa J, Ibe A (2006) Estimation of 1999–2004 dietary daily intake of PCDDs, PCDFs and dioxin-like PCBs by a total diet study in metropolitan Tokyo, Japan. Chemosphere 64:634–641CrossRefGoogle Scholar
  30. Tauchi M, Hida A, Negishi T, Katsuoka F, Noda S, Mimura J, Hosoya T, Yanaka A, Aburatani H, Fujii-Kuriyama Y, Motohashi H, Yamamoto M (2005) Constitutive expression of aryl hydrocarbon receptor in keratinocytes causes inflammatory skin lesions. Mol Cell Biol 25:9360–9368CrossRefGoogle Scholar
  31. ten Tusscher GW, Steerenberg PA, van Loveren H, Vos JG, von dem Borne AE, Westra M, van der Slikke JW, Olie K, Pluim HJ, Koppe JG (2003) Persistent hematologic and immunologic disturbances in 8-year-old Dutch children associated with perinatal dioxin exposure. Environ Health Perspect 111:1519–1523CrossRefGoogle Scholar
  32. Todaka T, Hirakawa H, Kajiwara J, Onozuka D, Sasaki S, Miyashita C, Yoshioka E, Yuasa M, Kishi R, Iida T, Uchi H, Furue M (2011) Concentrations of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and polychlorinated biphenyls in blood and breast milk collected from pregnant women in Sapporo City, Japan. Chemosphere 85:1694–1700CrossRefGoogle Scholar
  33. Tsukino H, Hanaoka T, Sasaki H, Motoyama H, Hiroshima M, Tanaka T, Kabuto M, Niskar AS, Rubin C, Patterson DG Jr, Turner W, Needham L, Tsugane S (2005) Associations between serum levels of selected organochlorine compounds and endometriosis in infertile Japanese women. Environ Res 99:118–125CrossRefGoogle Scholar
  34. Tsutsumi T, Yanagi T, Nakamura M, Kono Y, Uchibe H, Iida T, Hori T, Nakagawa R, Tobiishi K, Matsuda R, Sasaki K, Toyoda M (2001) Update of daily intake of PCDDs, PCDFs, and dioxin-like PCBs from food in Japan. Chemosphere 45:1129–1137CrossRefGoogle Scholar
  35. Uemura H, Arisawa K, Hiyoshi M, Kitayama A, Takami H, Sawachika F, Dakeshita S, Nii K, Satoh H, Sumiyoshi Y, Morinaga K, Kodama K, Suzuki T, Nagai M, Suzuki T (2009) Prevalence of metabolic syndrome associated with body burden levels of dioxin and related compounds among Japan’s general population. Environ Health Perspect 117:568–573Google Scholar
  36. van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, Rose M, Safe S, Schrenk D, Tohyama C, Tritscher A, Tuomisto J, Tysklind M, Walker N, Peterson RE (2006) The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93:223–241Google Scholar
  37. Wahn U, von Mutius E (2001) Childhood risk factors for atopy and the importance of early intervention. J Allergy Clin Immunol 107:567–574CrossRefGoogle Scholar
  38. Wang SL, Tsai PC, Yang CY, Leon Guo Y (2008) Increased risk of diabetes and polychlorinated biphenyls and dioxins: a 24-year follow-up study of the Yucheng cohort. Diabetes Care 31:1574–1579CrossRefGoogle Scholar
  39. Weisglas-Kuperus N (1998) Neurodevelopmental, immunological and endocrinological indices of perinatal human exposure to PCBs and dioxins. Chemosphere 37:1845–1853CrossRefGoogle Scholar
  40. Weisglas-Kuperus N, Patandin S, Berbers GA, Sas TC, Mulder PG, Sauer PJ, Hooijkaas H (2000) Immunologic effects of background exposure to polychlorinated biphenyls and dioxins in Dutch preschool children. Environ Health Perspect 108:1203–1207CrossRefGoogle Scholar
  41. Weisglas-Kuperus N, Vreugdenhil HJ, Mulder PG (2004) Immunological effects of environmental exposure to polychlorinated biphenyls and dioxins in Dutch school children. Toxicol Lett 149:281–285CrossRefGoogle Scholar
  42. WHO/IARC (1997) Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans. IARC monographs on the evaluation of carcinogenic risks to humans, vol 69Google Scholar
  43. Yu ML, Guo YL, Hsu CC, Rogan WJ (2000) Menstruation and reproduction in women with polychlorinated biphenyl (PCB) poisoning: long-term follow-up interviews of the women from the Taiwan Yucheng cohort. Int J Epidemiol 29:672–677CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Mariko Nakamoto
    • 1
    • 2
  • Kokichi Arisawa
    • 1
  • Hirokazu Uemura
    • 1
  • Sakurako Katsuura
    • 1
  • Hidenobu Takami
    • 1
  • Fusakazu Sawachika
    • 1
  • Miwa Yamaguchi
    • 1
  • Tomoya Juta
    • 1
  • Tohru Sakai
    • 2
  • Eisaku Toda
    • 3
  • Kei Mori
    • 3
  • Manabu Hasegawa
    • 3
  • Masaharu Tanto
    • 3
  • Masayuki Shima
    • 4
  • Yoshio Sumiyoshi
    • 4
  • Kenji Morinaga
    • 4
  • Kazunori Kodama
    • 4
  • Takaichiro Suzuki
    • 4
  • Masaki Nagai
    • 4
  • Hiroshi Satoh
    • 4
  1. 1.Department of Preventive Medicine, Institute of Health BiosciencesThe University of Tokushima Graduate SchoolTokushimaJapan
  2. 2.Department of Public Health and Applied Nutrition, Institute of Health BiosciencesThe University of Tokushima Graduate SchoolTokushimaJapan
  3. 3.Ministry of the Environment of JapanTokyoJapan
  4. 4.The Study Group of the Accumulation of Dioxins in HumansTokyoJapan

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