Abstract
This study explored effects of dietary OCP intake from plant-origin foods (cereals, fruits, and vegetables) consumption on lipid metabolism and inflammation of women using a multiple follow-up study. The results showed that dietary intake of p,p′-dichlorodiphenyltrichloroethane (DDT) [β = − 10.11, 95% confidence interval (95%CI): − 17.32, − 2.905] and o,p′-dichlorodiphenyldichloroethylene (DDE) (β = − 6.077, 95%CI: − 9.954, − 2.200) were overall negatively associated with serum high-density lipoprotein cholesterol (HDL), whereas other OCPs were not. Serum interleukin (IL)-8 was positively associated with intake of dieldrin (β = 0.390, 95%CI: 0.105, 0.674), endosulfan-β (β = 0.361, 95%CI: 0.198, 0.523), total endosulfan (β = 0.136, 95%CI: 0.037, 0.234), and total OCPs (β = 0.084, 95%CI: 0.016, 0.153), and negatively correlated with intake of p,p′-DDE (β = − 2.692, 95%CI: − 5.185, − 0.198). We concluded that dietary intake of some individual DDT-, DDE- dieldrin-, and endosulfan-class chemicals from plant-origin foods may interfere with lipid metabolism and inflammation responses.
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Aminov Z, Haase R, Olson JR, Pavuk M, Carpenter DO, Anniston Environmental Health Research Consortium (2014) Racial differences in levels of serum lipids and effects of exposure to persistent organic pollutants on lipid levels in residents of Anniston, Alabama. Environ Int 73:216–223. https://doi.org/10.1016/j.envint.2014.07.022
Aminov Z, Carpenter DO (2020) Serum concentrations of persistent organic pollutants and the metabolic syndrome in Akwesasne Mohawks, a Native American community. Environ Pollut 260:114004. https://doi.org/10.1016/j.envpol.2020.114004
Calder PC, Ahluwalia N, Brouns F, Buetler T, Clement K, Cunningham K, Esposito K, Jonsson LS, Kolb H, Lansink M, Marcos A, Margioris A, Matusheski N, Nordmann H, O’Brien J, Pugliese G, Rizkalla S, Schalkwijk C, Tuomilehto J, Warnberg J, Watzl B, Winklhofer-Roob BM (2011) Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr 106(Suppl 3):S5–78. https://doi.org/10.1017/S0007114511005460
Castro-Barquero S, Ruiz-Leon AM, Sierra-Perez M, Estruch R, Casas R (2020) Dietary strategies for metabolic syndrome: a comprehensive review. Nutrients 12:2983. https://doi.org/10.3390/nu12102983
Cecilia Tellez-Banuelos M, Haramati J, Franco-Topete K, Peregrina-Sandoval J, Franco-Topete R, Zaitseva GP (2016) Chronic exposure to endosulfan induces inflammation in murine colon via β-catenin expression and IL-6 production. J Immunotoxicol 13:842–849. https://doi.org/10.1080/1547691x.2016.1206998
Chen YC, Zang L, Shen GF, Liu MD, Du W, Fei J, Yang LY, Chen L, Wang XJ, Liu WP, Zhao MR (2019) Resolution of the ongoing challenge of estimating nonpoint source neonicotinoid pollution in the Yangtze river basin using a modified mass balance approach. Environ Sci Technol 53:2539–2548. https://doi.org/10.1021/acs.est.8b06096
Chen JX, Lan CX, An H, Jin Y, Li Q, Ge SF, Yu YX, Shen GF, Pan B, Xu Y, Ye RW, Li ZW, Wang B (2020) Potential interference on the lipid metabolisms by serum copper in a women population: a repeated measurement study. Sci Total Environ 760:143375. https://doi.org/10.1016/j.scitotenv.2020.143375
Dusanov S, Ruzzin J, Kiviranta H, Klemsdal TO, Retterstol L, Rantakokko P, Airaksinen R, Djurovic S, Tonstad S (2018) Associations between persistent organic pollutants and metabolic syndrome in morbidly obese individuals. Nutr Metab Carbiovasc Dis 28:735–742. https://doi.org/10.1016/j.numecd.2018.03.004
Greten FR, Grivennikov SI (2019) Inflammation and cancer: triggers, mechanisms, and consequences. Immunity 51:27–41. https://doi.org/10.1016/j.immuni.2019.06.025
Han X, Zhang F, Meng LL, Xu YD, Li YM, Li A, Turyk ME, Yang RQ, Wang P, Zhang JQ, Zhang QH, Jiang GB (2020) Exposure to organochlorine pesticides and the risk of type 2 diabetes in the population of East China. Ecotox Environ Safe 190:110125. https://doi.org/10.1016/j.ecoenv.2019.110125
Herst PM, Aars J, Joly Beauparlant C, Bodein A, Dalvai M, Gagne D, Droit A, Bailey JL, Routti H (2020) Adipose tissue transcriptome is related to pollutant exposure in polar bear mother-cub Pairs from Svalbard, Norway. Environ Sci Technol 54:11365–11375. https://doi.org/10.1021/acs.est.0c01920
Huang YC, Fang ML (2020) Nutritional and environmental contaminant exposure: a tale of two co-existing factors for disease risks. Environ Sci Technol 54:14793–14796. https://doi.org/10.1021/acs.est.0c05658
Jang TC, Jang JH, Lee KW (2016) Mechanism of acute endosulfan intoxication-induced neurotoxicity in sprague-Dawley rats. Arh Hig Rada Toksikol 67:9–17. https://doi.org/10.1515/aiht-2016-67-2702
Ko E, Choi M, Shin S (2020) Bottom-line mechanism of organochlorine pesticides on mitochondria dysfunction linked with type 2 diabetes. J Hazard Mater 393:122400. https://doi.org/10.1016/j.jhazmat.2020.122400
Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, Jacobs DR Jr (2011) Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes. PLoS ONE 6:e15977. https://doi.org/10.1371/journal.pone.0015977
Li S, Xu D, Guo JG, Sun YQ (2016) Inhibition of cell growth and induction of inflammation by endosulfan in HUVEC-C cells. Environ Toxicol 31:1785–1795. https://doi.org/10.1002/tox.22180
Lippitz BE (2013) Cytokine patterns in patients with cancer: a systematic review. Lancet Oncol 14:e218–228. https://doi.org/10.1016/s1470-2045(12)70582-x
Mustafa M, Garg N, Banerjee BD, Sharma T, Tyagi V, Dar SA, Guleria K, Ahmad RS, Vaid N, Tripathi AK (2015) Inflammatory-mediated pathway in association with organochlorine pesticides levels in the etiology of idiopathic preterm birth. Reprod Toxicol 57:111–120. https://doi.org/10.1016/j.reprotox.2015.05.018
Patel CJ, Cullen MR, Ioannidis JP, Butte AJ (2012) Systematic evaluation of environmental factors: persistent pollutants and nutrients correlated with serum lipid levels. Int J Epidemiol 41:828–843. https://doi.org/10.1093/ije/dys003
Peinado FM, Artacho-Cordon F, Barrios-Rodriguez R, Arrebola JP (2020) Influence of polychlorinated biphenyls and organochlorine pesticides on the inflammatory milieu. A systematic review of in vitro, in vivo and epidemiological studies. Environ Res 186:109561. https://doi.org/10.1016/j.envres.2020.109561
Ren MY, Pei RJ, Jiangtulu BHBK, Chen JX, Xue T, Shen GF, Yuan XR, Li KX, Lan CX, Chen Z, Chen XW, Wang Y, Jia XQ, Li ZW, Rashid A, Prapamontol T, Zhao XG, Dong ZM, Zhang YL, Zhang L, Ye RW, Li ZW, Guan WX, Wang B (2021) Contribution of temperature increase to restrain the transmission of COVID-19. Innovation (New York) 2:100071. https://doi.org/10.1016/j.xinn.2020.100071
Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, Lillefosse H, Ma T, Pesenti S, Sonne SB, Marstrand TT, Malde MK, Du ZY, Chavey C, Fajas L, Lundebye AK, Brand CL, Vidal H, Kristiansen K, Froyland L (2010) Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect 118:465–471. https://doi.org/10.1289/ehp.0901321
Salihovic S, Ganna A, Fall T, Broeckling CD, Prenni JE, van Bavel B, Lind PM, Ingelsson E, Lind L (2016) The metabolic fingerprint of p, p’-DDE and HCB exposure in humans. Environ Int 88:60–66. https://doi.org/10.1016/j.envint.2015.12.015
Shah HK, Sharma T, Banerjee BD (2020) Organochlorine pesticides induce inflammation, ROS production, and DNA damage in human epithelial ovary cells: an in vitro study. Chemosphere 246:125691. https://doi.org/10.1016/j.chemosphere.2019.125691
Shin PK, Park SJ, Kim MS, Kwon DY, Kim MJ, Kim K, Chun S, Lee HJ, Choi SW (2020) A traditional Korean diet with a low dietary inflammatory index increases anti-inflammatory IL-10 and decreases pro-inflammatory NF-κB in a small dietary intervention study. Nutrients 12:2468. https://doi.org/10.3390/nu12082468
Thorburn AN, Macia L, Mackay CR (2014) Diet, metabolites, and “Western-lifestyle” inflammatory diseases. Immunity 40:833–842. https://doi.org/10.1016/j.immuni.2014.05.014
Tsai S-J (2021) Role of interleukin 8 in depression and other psychiatric disorders. Prog Neuro-Psychopharmacol Biol Psychiatry 106:110173–110173. https://doi.org/10.1016/j.pnpbp.2020.110173
UNEP (2019) Stockholm Convention on Persistent Organic Pollutant (POPs). http://chm.pops.int/TheConvention/ThePOPs/tabid/673/Default.aspx.. Accessed 16 Dec 2020
Xi BD, Yu MD, Zhang Y, Gao RT, Zhang H, Li D, Tan WB, Hou HB, Yu H (2016) Residues and health risk assessments of organochlorine pesticides in a typical wastewater irrigation area of North China. Asian J Ecotoxicol 11:453–464. https://doi.org/10.7524/AJE.1673-5897.20151019001
Xu XH, Dailey AB, Talbott EO, Ilacqua VA, Kearney G, Asal NR (2010) Associations of serum concentrations of organochlorine pesticides with breast cancer and prostate cancer in US adults. Environ Health Perspect 118:60–66. https://doi.org/10.1289/ehp.0900919
Yu YX, Li CL, Zhang XL, Zhang XY, Pang YP, Zhang SH, Fu JM (2012) Route-specific daily uptake of organochlorine pesticides in food, dust, and air by Shanghai residents, China. Environ Int 50:31–37. https://doi.org/10.1016/j.envint.2012.09.007
Yu HY, Liu YF, Shu XQ, Ma LM, Pan YW (2020) Assessment of the spatial distribution of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) in urban soil of China. Chemosphere 243:125392. https://doi.org/10.1016/j.chemosphere.2019.125392
Zhang QQ, Xia ZH, Wu MM, Wang LP, Yang H (2017) Human health risk assessment of DDTs and HCHs through dietary exposure in Nanjing, China. Chemosphere 177:211–216. https://doi.org/10.1016/j.chemosphere.2017.03.003
Acknowledgments
All authors would like to express our gratitude to the help from the working group of environmental exposure and human health of the China Cohort Consortium (See http://chinacohort.bjmu.edu.cn/). This work was supported by the National Natural Science Foundation of China (Grant Nos. 41401583, 41771527, and 41922057).
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Wang, X., Gao, M., Tan, Y. et al. Associations of Dietary Exposure to Organochlorine Pesticides from Plant-Origin Foods with Lipid Metabolism and Inflammation in Women: A Multiple Follow-up Study in North China. Bull Environ Contam Toxicol 107, 289–295 (2021). https://doi.org/10.1007/s00128-021-03224-5
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DOI: https://doi.org/10.1007/s00128-021-03224-5