DOI QR코드

DOI QR Code

Association between food consumption and serum aryl hydrocarbon receptor ligand activity among middle-aged Korean adults

  • Kyungho Ha (Department of Food Science and Nutrition, Jeju National University) ;
  • Hoonsung Choi (Department of Internal Medicine, Chung-Ang University College of Medicine) ;
  • Youngmi Kim Pak (Department of Physiology, College of Medicine and Biomedical Science Institute, Core Research Institute(CRI), School of Medicine, Kyung Hee University) ;
  • Hong Kyu Lee (Department of Internal Medicine, Seoul National University College of Medicine) ;
  • Hyojee Joung (Department of Public Health, Graduate School of Public Health, Seoul National University)
  • Received : 2024.05.21
  • Accepted : 2024.08.05
  • Published : 2024.10.01

Abstract

BACKGROUND/OBJECTIVES: The diet is an important route of exposure to endocrine-disrupting chemicals (EDCs). However, few studies have investigated the association between dietary intake and EDC exposure levels among Koreans. In an earlier study, we showed that the bioactivity of serum aryl hydrocarbon receptor ligands (AhRLs) could be a surrogate biomarker to indicate exposure to EDCs and that they inhibit mitochondrial function. We also found that the mitochondria-inhibiting substances (MIS) in serum ascertained by intracellular adenosine triphosphate (MIS-ATP) and reactive oxygen species (MIS-ROS) levels could be biomarkers of exposure to EDCs, as they showed a strong correlation with AhRL and the levels of EDCs in the blood. Here, we investigated the association between the consumption of specific foods and surrogate serum biomarkers for EDCs, namely AhRL, MIS-ATP, and MIS-ROS, among middle-aged Korean adults. SUBJECTS/METHODS: A total of 1,466 participants aged 45-76 yrs from the Ansung cohort of the Korean Genome and Epidemiology Study were included. Food consumption, including that of meat, fish, vegetables, and fruits, was measured using a semiquantitative food frequency questionnaire. RESULTS: Fish intake was positively associated with AhRL (β = 0.0035, P = 0.0166), whereas cruciferous vegetable intake was negatively associated with AhRL (β = -0.0007, P = 0.0488). Cruciferous vegetable intake was positively associated with the MIS-ATP levels (β = 0.0051, P = 0.0420). A higher intake of fish was significantly associated with an increased risk of high AhRL (tertile: odds ratio [OR], 1.49; 95% confidence intervals (CIs), 1.08-2.06; P for trend = 0.0305). In addition, the second-highest tertile of cruciferous vegetable intake had lower odds of high AhRL than the lowest tertile (OR, 0.73; 95% CIs, 0.54-0.97), although no significant linear trend was observed. CONCLUSION: Consumption of different types of foods may be differentially associated with EDC exposure in middle-aged Korean adults.

Keywords

Acknowledgement

This research was supported by the Basic Science Research Program (Core Research Institute Program 2018R1A6A1A03025124 and 2020R1A2C1008699 to Pak YK) through the National Research Foundation of Korea (NRF), funded by the Korean government (MSIT) and Gyeokin Health Science to Joung H. The funding sources had no role in the collection of data or decision to submit this manuscript for publication.

References

  1. Song Y, Chou EL, Baecker A, You NC, Song Y, Sun Q, Liu S. Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: a systematic review and meta-analysis. J Diabetes 2016;8:516-32.
  2. Heindel JJ, Blumberg B, Cave M, Machtinger R, Mantovani A, Mendez MA, Nadal A, Palanza P, Panzica G, Sargis R, et al. Metabolism disrupting chemicals and metabolic disorders. Reprod Toxicol 2017;68:3-33.
  3. Le Magueresse-Battistoni B, Vidal H, Naville D. Environmental pollutants and metabolic disorders: the multi-exposure scenario of life. Front Endocrinol (Lausanne) 2018;9:582.
  4. Ribeiro CM, Beserra BT, Silva NG, Lima CL, Rocha PR, Coelho MS, Neves FA, Amato AA. Exposure to endocrine-disrupting chemicals and anthropometric measures of obesity: a systematic review and meta-analysis. BMJ Open 2020;10:e033509.
  5. Windal I, Denison MS, Birnbaum LS, Van Wouwe N, Baeyens W, Goeyens L. Chemically activated luciferase gene expression (CALUX) cell bioassay analysis for the estimation of dioxin-like activity: critical parameters of the CALUX procedure that impact assay results. Environ Sci Technol 2005;39:7357-64.
  6. Murray IA, Patterson AD, Perdew GH. Aryl hydrocarbon receptor ligands in cancer: friend and foe. Nat Rev Cancer 2014;14:801-14.
  7. Park WH, Jun DW, Kim JT, Jeong JH, Park H, Chang YS, Park KS, Lee HK, Pak YK. Novel cell-based assay reveals associations of circulating serum AhR-ligands with metabolic syndrome and mitochondrial dysfunction. Biofactors 2013;39:494-504.
  8. Lee HK, Park WH, Kang YC, Kang S, Im S, Park S, Kim JT, Lee M, Seok J, Oh MS, et al. Serum biomarkers from cell-based assays for AhRL and MIS strongly predicted the future development of diabetes in a large community-based prospective study in Korea. Sci Rep 2020;10:6339.
  9. Park WH, Kang S, Lee HK, Salihovic S, Bavel BV, Lind PM, Pak YK, Lind L. Relationships between serum-induced AhR bioactivity or mitochondrial inhibition and circulating polychlorinated biphenyls (PCBs). Sci Rep 2017;7:9383.
  10. Park S, Chon S, Park SY, Yun S, Baik SH, Woo JT, Rhee SY, Pak YK, Kim SH. Association of aryl hydrocarbon receptor transactivating activity, a potential biomarker for persistent organic pollutants, with the risk of gestational diabetes mellitus. Sci Rep 2021;11:3185.
  11. Guo W, Pan B, Sakkiah S, Yavas G, Ge W, Zou W, Tong W, Hong H. Persistent organic pollutants in food: contamination sources, health effects and detection methods. Int J Environ Res Public Health 2019;16:4361.
  12. Mukherjee R, Pandya P, Baxi D, Ramachandran AV. Endocrine disruptors-'food' for thought. Proc Zool Soc 2021;74:432-42.
  13. Li Y, Innocentin S, Withers DR, Roberts NA, Gallagher AR, Grigorieva EF, Wilhelm C, Veldhoen M. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 2011;147:629-40.
  14. Hooper LV. You AhR what you eat: linking diet and immunity. Cell 2011;147:489-91.
  15. Donovan MG, Selmin OI, Romagnolo DF. Aryl hydrocarbon receptor diet and breast cancer risk. Yale J Biol Med 2018;91:105-27.
  16. Kim Y, Han BG; KoGES Group. Cohort profile: the Korean Genome and Epidemiology Study (KoGES) consortium. Int J Epidemiol 2017;46:1350.
  17. The Korean Nutrition Society. Food composition table. In: Recommended Dietary Allowances for Koreans. 7th ed. Seoul: Korean Nutrition Society; 2000. 
  18. Kim JT, Lee HK. Metabolic syndrome and the environmental pollutants from mitochondrial perspectives. Rev Endocr Metab Disord 2014;15:253-62.
  19. Korashy HM, El-Kadi AO. Differential effects of mercury, lead and copper on the constitutive and inducible expression of aryl hydrocarbon receptor (AHR)-regulated genes in cultured hepatoma Hepa 1c1c7 cells. Toxicology 2004;201:153-72.
  20. Amara IE, Anwar-Mohamed A, Abdelhamid G, El-Kadi AO. Effect of mercury on aryl hydrocarbon receptor-regulated genes in the extrahepatic tissues of C57BL/6 mice. Food Chem Toxicol 2012;50:2325-34.
  21. Kulas J, Tucovic D, Zeljkovic M, Popovic D, Popov Aleksandrov A, Kataranovski M, Mirkov I. Aryl hydrocarbon receptor is involved in the proinflammatory cytokine response to cadmium. Biomed Environ Sci 2021;34:192-202.
  22. De Juan A, Segura E. Modulation of immune responses by nutritional ligands of aryl hydrocarbon receptor. Front Immunol 2021;12:645168.
  23. Rimm EB, Appel LJ, Chiuve SE, Djousse L, Engler MB, Kris-Etherton PM, Mozaffarian D, Siscovick DS, Lichtenstein AH, et al.; American Heart Association Nutrition Committee of the Council on Lifestyle and Cardiometabolic Health Seafood long-chain n-3 polyunsaturated fatty acids and cardiovascular disease: a science advisory from the American Heart Association. Circulation 2018;138:e35-47.
  24. Ministry of Health and Welfare (KR); The Korean Nutrition Society. Dietary Reference Intakes for Koreans 2020. Sejong: Ministry of Health and Welfare; 2020. 
  25. US Department of Agriculture; US Department of Health and Human Services. Dietary Guidelines for Americans; 2020-2025. 9th ed. Washington, D.C.: US Department of Agriculture; 2020. 
  26. Schecter A, Papke O, Harris TR, Tung KC, Musumba A, Olson J, Birnbaum L. Polybrominated diphenyl ether (PBDE) levels in an expanded market basket survey of U.S. food and estimated PBDE dietary intake by age and sex. Environ Health Perspect 2006;114:1515-20.
  27. US Food and Drug Administration; US Environmental Protection Agency. Advice about eating fish [Internet]. Silver Spring (MD): US Food and Drug Administration; 2021 [cited 2024 February 28]. Available from: https://www.fda.gov/food/consumers/advice-about-eating-fish. 
  28. Li A, Tang Q, Kearney KE, Nagy KL, Zhang J, Buchanan S, Turyk ME. Persistent and toxic chemical pollutants in fish consumed by Asians in Chicago, United States. Sci Total Environ 2022;811:152214.
  29. Pironti C, Ricciardi M, Proto A, Bianco PM, Montano L, Motta O. Endocrine-disrupting compounds: an overview on their occurrence in the aquatic environment and human exposure. Water 2021;13:1347.
  30. Jeong Y, Lee Y, Park KJ, An YR, Moon HB. Accumulation and time trends (2003-2015) of persistent organic pollutants (POPs) in blubber of finless porpoises (Neophocaena asiaeorientalis) from Korean coastal waters. J Hazard Mater 2020;385:121598.
  31. Riaz R, de Wit CA, Malik RN. Persistent organic pollutants (POPs) in fish species from different lakes of the lesser Himalayan region (LHR), Pakistan: the influence of proximal sources in distribution of POPs. Sci Total Environ 2021;760:143351.
  32. Awata H, Linder S, Mitchell LE, Delclos GL. Association of dietary intake and biomarker levels of arsenic, cadmium, lead, and mercury among Asian populations in the United States: NHANES 2011-2012. Environ Health Perspect 2017;125:314-23.
  33. Terry AL, Herrick KA, Afful J, Ahluwalia N. Seafood consumption in the United States, 2013-2016. NCHS Data Brief 2018;321:1-8.
  34. Jeon HL, Hong S, Choi K, Lee C, Yoo J. First nationwide exposure profile of major persistent organic pollutants among Korean adults and their determinants: Korean National Environmental Health Survey Cycle 3 (2015-2017). Int J Hyg Environ Health 2021;236:113779.
  35. Kodavanti PR, Royland JE, Rao Sambasiva KR. Toxicology of persistent organic pollutants. In: Reference Module in Biomedical Science. Amsterdam: Elsevier; 2014. 
  36. Vaccher V, Ingenbleek L, Adegboye A, Hossou SE, Kone AZ, Oyedele AD, Kisito CS, Dembele YK, Hu R, Adbel Malak I, et al. Levels of persistent organic pollutants (POPs) in foods from the first regional Sub-Saharan Africa Total Diet Study. Environ Int 2020;135:105413.
  37. Domingo JL. Concentrations of environmental organic contaminants in meat and meat products and human dietary exposure: a review. Food Chem Toxicol 2017;107:20-6.
  38. Ha K, Joung H, Song Y. Inadequate fat or carbohydrate intake was associated with an increased incidence of type 2 diabetes mellitus in Korean adults: a 12-year community-based prospective cohort study. Diabetes Res Clin Pract 2019;148:254-61.