{"paper_id":"8d2782ff-168b-436b-b47d-6229c6457a90","body_text":"Abstract\nTo explore the association between exposure to polycyclic aromatic hydrocarbons (PAHs) and endometriosis risk. Data were obtained from the 2003–2006 National Health and Nutrition Examination Survey database. Urinary concentrations of PAHs were divided into quartiles, and weighted multivariate logistic regression, restricted cubic spline, and subgroup analyses were performed. An extreme gradient boosting (XGBoost) algorithm was used to screen the most important PAHs. After multivariable adjustments, 9-fluorene, 1-phenanthrene, 2-phenanthrene, and 4-phenanthrene exposure were significantly associated with a risk of endometriosis. Specifically, compared with the reference group, the odds ratios (ORs) of endometriosis for the fourth quartile were 3.52 (95% confidence interval (CI): 1.15, 10.77), 3.10 (95% CI: 1.37, 6.97), 4.86 (95% CI: 1.93, 12.21), and 2.67 (95% CI: 1.02, 7.01) for 9-fluorene, 1-phenanthrene, 2-phenanthrene, and 4-phenanthrene, respectively. In terms of continuous exposure, each one-standard-deviation increase in the urinary concentration of 9-fluorene, 1-phenanthrene, 2-phenanthrene, and 4-phenanthrene was independently associated with a 66% (OR: 1.66, 95% CI: 1.15, 2.40), 62% (OR:1.62, 95% CI: 1.19, 2.20), 68% (OR: 1.68, 95% CI: 1.24, 2.28), and 56% (OR: 1.56, 95% CI: 1.11, 2.19) increase in the risk of endometriosis, respectively, in the fully adjusted model. A significant association between the urinary concentration of 9-fluorene and the risk of endometriosis was also observed in participants who had a high body-mass index (≥25 kg/m2), with a corresponding OR of 2.61 (95% CI: 1.37, 5.00; P for interaction = 0.006). Our findings show that high urinary concentrations of PAHs were associated with a high risk of endometriosis in participants and that the urinary concentration of 9-fluorene was related with a high susceptibility of endometriosis in participants with overweight.\nSimilar content being viewed by others\nData availability\nObtaining data from corresponding authors with appropriate justification.\nReferences\nBock KW, Köhle C (2006) Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 72:393–404. https://doi.org/10.1016/j.bcp.2006.01.017\nBoffetta P, Jourenkova N, Gustavsson P (1997) Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control : Ccc 8:444–472. https://doi.org/10.1023/a:1018465507029\nBolden AL, Rochester JR, Schultz K, Kwiatkowski CF (2017) Polycyclic aromatic hydrocarbons and female reproductive health: a scoping review. Reprod Toxicol (Elmsford, NY) 73:61–74. https://doi.org/10.1016/j.reprotox.2017.07.012\nBorman SM, Christian PJ, Sipes IG, Hoyer PB (2000) Ovotoxicity in female Fischer rats and B6 mice induced by low-dose exposure to three polycyclic aromatic hydrocarbons: comparison through calculation of an ovotoxic index. Toxicol Appl Pharmacol 167:191–198. https://doi.org/10.1006/taap.2000.9006\nBulun SE, Zeitoun KM, Kilic G (2000) Expression of dioxin-related transactivating factors and target genes in human eutopic endometrial and endometriotic tissues. Am J Obstet Gynecol 182:767–775. https://doi.org/10.1016/s0002-9378(00)70325-5\nBurney RO, Giudice LC (2012) Pathogenesis and pathophysiology of endometriosis. Fertil Steril 98:511–519. https://doi.org/10.1016/j.fertnstert.2012.06.029\nChapron C et al (2010) Smoking habits of 411 women with histologically proven endometriosis and 567 unaffected women. Fertil Steril 94:2353–2355. https://doi.org/10.1016/j.fertnstert.2010.04.020\nCzyzyk A, Podfigurna A, Szeliga A, Meczekalski B (2017) Update on endometriosis pathogenesis. Minerva Ginecol 69:447-461 .https://doi.org/10.23736/s0026-4784.17.04048-5\nDahlstrom D, Bloomhuff A (2014) ACGIH® (American conference of governmental industrial hygienists) 178–179. https://doi.org/10.1016/b978-0-12-386454-3.00584-4\nDe Felip E, Porpora MG, di Domenico A, Ingelido AM, Cardelli M, Cosmi EV, Donnez J (2004) Dioxin-like compounds and endometriosis: a study on Italian and Belgian women of reproductive age. Toxicol Lett 150:203–209. https://doi.org/10.1016/j.toxlet.2004.01.008\nDiggs DL et al (2011) Polycyclic aromatic hydrocarbons and digestive tract cancers: a perspective Journal of environmental science and health Part C. Environ Carcinog Ecotoxicol Rev 29:324–357. https://doi.org/10.1080/10590501.2011.629974\nDuleba AJ (1997) Diagnosis of endometriosis. Obstet Gynecol Clin N Am 24:331–346. https://doi.org/10.1016/s0889-8545(05)70307-7\nGao P, da Silva E, Hou L, Denslow ND, Xiang P, Ma LQ (2018) Human exposure to polycyclic aromatic hydrocarbons: metabolomics perspective. Environ Int 119:466–477. https://doi.org/10.1016/j.envint.2018.07.017\nGündoğdu S (2023) Efficient prediction of early-stage diabetes using XGBoost classifier with random forest feature selection technique. Multimedia Tools Appl:1–19. https://doi.org/10.1007/s11042-023-15165-8\nGuo J, Wang C, Guo Z, Zuo Z (2018) Exposure to environmental level phenanthrene induces a NASH-like phenotype in new born rat. Environ Pollut (Barking, Essex : 1987) 239:261–271. https://doi.org/10.1016/j.envpol.2018.04.030\nHernández-Ochoa I, Karman BN, Flaws JA (2009) The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem Pharmacol 77:547–559. https://doi.org/10.1016/j.bcp.2008.09.037\nHouston DE (1984) Evidence for the risk of pelvic endometriosis by age, race and socioeconomic status. Epidemiol Rev 6:167–191. https://doi.org/10.1093/oxfordjournals.epirev.a036270\nIfegwu OC, Anyakora C (2015) Polycyclic aromatic hydrocarbons: part I. Exposure. Adv Clin Chem 72:277–304. https://doi.org/10.1016/bs.acc.2015.08.001\nJiang YZ, Wang K, Fang R, Zheng J (2010) Expression of aryl hydrocarbon receptor in human placentas and fetal tissues. J Histochem Cytochem 58:679–685. https://doi.org/10.1369/jhc.2010.955955\nJohnson CL, Paulose-Ram R, Ogden CL, Carroll MD, Kruszon-Moran D, Dohrmann SM, Curtin LR (2013) National health and nutrition examination survey: analytic guidelines, 1999-2010. Vital Health Stat 2(161):1–24\nKummer V, Masková J, Zralý Z, Neca J, Simecková P, Vondrácek J, Machala M (2008) Estrogenic activity of environmental polycyclic aromatic hydrocarbons in uterus of immature. Wistar rats Toxicology letters 180:212–221. https://doi.org/10.1016/j.toxlet.2008.06.862\nLi F et al (2020) Hepatotoxic effects of inhalation exposure to polycyclic aromatic hydrocarbons on lipid metabolism of C57BL/6 mice. Environ Int 134:105000. https://doi.org/10.1016/j.envint.2019.105000\nLi Z et al (2006) Measurement of urinary monohydroxy polycyclic aromatic hydrocarbons using automated liquid-liquid extraction and gas chromatography/isotope dilution high-resolution mass spectrometry. Anal Chem 78:5744–5751. https://doi.org/10.1021/ac0606094\nMarquardt RM, Kim TH, Shin, JH, Jeong JW (2019) Progesterone and estrogen signaling in the endometrium: What Goes Wrong in Endometriosis? Int J Mol Sci 20(15). https://doi.org/10.3390/ijms20153822\nMcLeod BS, Retzloff MG (2010) Epidemiology of endometriosis: an assessment of risk factors. Clin Obstet Gynecol 53:389–396. https://doi.org/10.1097/GRF.0b013e3181db7bde\nMehta M, Julaiti J, Griffin P, Kumara S (2020) Early stage machine learning-based prediction of US county vulnerability to the COVID-19 pandemic: machine learning approach. JMIR Public Health Surveill 6:e19446. https://doi.org/10.2196/19446\nMissmer SA, Cramer DW (2003) The epidemiology of endometriosis Obstetrics and gynecology. Clinics of North Am 30(1-19):vii. https://doi.org/10.1016/s0889-8545(02)00050-5\nMoini A, Malekzadeh F, Amirchaghmaghi E, Kashfi F, Akhoond MR, Saei M, Mirbolok MH (2013) Risk factors associated with endometriosis among infertile Iranian women. Arch Med Sci : AMS 9:506–514. https://doi.org/10.5114/aoms.2013.35420\nOlsson AC et al (2010) Occupational exposure to polycyclic aromatic hydrocarbons and lung cancer risk: a multicenter study in Europe. Occup Environ Med 67:98–103. https://doi.org/10.1136/oem.2009.046680\nPeters JM, Narotsky MG, Elizondo G, Fernandez-Salguero PM, Gonzalez FJ, Abbott BD (1999) Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-null mice. Toxicol Sci : An Official J Soc Toxicol 47:86–92. https://doi.org/10.1093/toxsci/47.1.86\nRamesh A, Inyang F, Hood DB, Archibong AE, Knuckles ME, Nyanda AM (2001) Metabolism, bioavailability, and toxicokinetics of benzo(alpha)pyrene in F-344 rats following oral administration. Exp Toxicol Pathol : Official J Gesellschaft Fur Toxikologische Pathologie 53:275–290. https://doi.org/10.1078/0940-2993-00192\nRomanoff LC, Li Z, Young KJ, Blakely NC 3rd, Patterson DG Jr, Sandau CD (2006) Automated solid-phase extraction method for measuring urinary polycyclic aromatic hydrocarbon metabolites in human biomonitoring using isotope-dilution gas chromatography high-resolution mass spectrometry. J Cchromatog B Anal Technol Biomed Life Sci 835:47–54. https://doi.org/10.1016/j.jchromb.2006.03.004\nRowlands IJ, Hockey R, Abbott JA, Montgomery GW, Mishra GD (2022) Body mass index and the diagnosis of endometriosis: findings from a national data linkage cohort study. Obes Res Clin Pract 16:235–241. https://doi.org/10.1016/j.orcp.2022.04.002\nRumph JT, Stephens VR, Archibong AE, Osteen KG, Bruner-Tran KL (2020) Environmental endocrine disruptors and endometriosis. Adv Anat Embryol Cell Biol 232:57–78. https://doi.org/10.1007/978-3-030-51856-1_4\nSadeu JC, Hughes CL, Agarwal S, Foster WG (2010) Alcohol, drugs, caffeine, tobacco, and environmental contaminant exposure: reproductive health consequences and clinical implications. Crit Rev Toxicol 40:633–652. https://doi.org/10.3109/10408444.2010.493552\nScheurer ME, Danysh HE, Follen M, Lupo PJ (2014) Association of traffic-related hazardous air pollutants and cervical dysplasia in an urban multiethnic population: a cross-sectional study. Environ Health : a Glob Access Sci Source 13:52. https://doi.org/10.1186/1476-069x-13-52\nStockinger B, Di Meglio P, Gialitakis M, Duarte JH (2014) The aryl hydrocarbon receptor: multitasking in the immune system. Annu Rev Immunol 32:403–432. https://doi.org/10.1146/annurev-immunol-032713-120245\nSverdrup LE, Nielsen T, Krogh PH (2002) Soil ecotoxicity of polycyclic aromatic hydrocarbons in relation to soil sorption, lipophilicity, and water solubility. Environ Sci Technol 36:2429–2435. https://doi.org/10.1021/es010180s\nUnwin J, Cocker J, Scobbie E, Chambers H (2006) An assessment of occupational exposure to polycyclic aromatic hydrocarbons in the UK. Ann Occup Hyg 50:395–403. https://doi.org/10.1093/annhyg/mel010\nVercellini P, Viganò P, Somigliana E, Fedele L (2014) Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol 10:261–275. https://doi.org/10.1038/nrendo.2013.255\nWang M, Jia S, Lee SH, Chow A, Fang M (2021) Polycyclic aromatic hydrocarbons (PAHs) in indoor environments are still imposing carcinogenic risk. J Hazard Mater 409:124531. https://doi.org/10.1016/j.jhazmat.2020.124531\nZhong Y et al (2011) Immediate consequences of cigarette smoking: rapid formation of polycyclic aromatic hydrocarbon diol epoxides. Chem Res Toxicol 24:246–252. https://doi.org/10.1021/tx100345x\nAcknowledgements\nWe thank all the participants in the study.\nAuthor information\nAuthors and Affiliations\nContributions\nB.W., H.Z., and X.Z. conceived and designed the study. B.W., J.W., and H.W. analyzed and interpreted the data. B.W. and H.Z. drafted the manuscript. X.Z. contributed to the interpretation of the results. J.J. assisted with the data collection and analysis. All authors agreed to be accountable for all aspects of the work. All authors contributed to the article and approved the submitted version.\nCorresponding author\nEthics declarations\nEthical approval\nNHANES Institutional Review Board approved the ethical conduct of NHANES 2003–2006.\nConsent to participate\nEvery participant signed an informed consent form.\nConsent for publication\nNot applicable.\nConflict of interest\nThe authors declare no competing interests.\nAdditional information\nResponsible Editor: Lotfi Aleya\nPublisher’s note\nSpringer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.\nRights and permissions\nSpringer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.\nAbout this article\nCite this article\nWang, B., Zhang, H., Zhang, X. et al. Association between urinary concentrations of polycyclic aromatic hydrocarbons and risk of endometriosis in the NHANES 2003–2006. Environ Sci Pollut Res 30, 117715–117728 (2023). https://doi.org/10.1007/s11356-023-30545-1\nReceived:\nAccepted:\nPublished:\nVersion of record:\nIssue date:\nDOI: https://doi.org/10.1007/s11356-023-30545-1","source_license":"CC0","license_restricted":false}