Association between urinary concentrations of polycyclic aromatic hydrocarbons and risk of endometriosis in the NHANES 2003-2006

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Higher urinary concentrations of 9-fluorene, 1-phenanthrene, 2-phenanthrene, and 4-phenanthrene were associated with increased endometriosis risk, particularly 9-fluorene in overweight individuals.

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This study used NHANES 2003–2006 data to assess whether urinary polycyclic aromatic hydrocarbons (PAHs) are associated with endometriosis risk, using weighted multivariable logistic regression, restricted cubic splines, subgroup analyses, and an XGBoost-based screening of the most important PAHs. After full adjustment, higher urinary levels of 9-fluorene, 1-phenanthrene, 2-phenanthrene, and 4-phenanthrene were significantly associated with increased odds of endometriosis, with odds ratios for the highest quartile ranging from 2.67 to 4.86 and per standard-deviation increases also showing positive associations. A significant interaction was reported for 9-fluorene, where the association with endometriosis persisted among participants with BMI ≥25 kg/m². This paper is centrally about endometriosis — it investigates urinary PAH concentrations and endometriosis risk using NHANES 2003–2006.

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Abstract

To 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.
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Abstract

To 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. Similar content being viewed by others Data availability Obtaining data from corresponding authors with appropriate justification.

References

Bock 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 Boffetta 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 Bolden 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 Borman 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 Bulun 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 Burney RO, Giudice LC (2012) Pathogenesis and pathophysiology of endometriosis. Fertil Steril 98:511–519. https://doi.org/10.1016/j.fertnstert.2012.06.029 Chapron 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 Czyzyk 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 Dahlstrom 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 De 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 Diggs 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 Duleba AJ (1997) Diagnosis of endometriosis. Obstet Gynecol Clin N Am 24:331–346. https://doi.org/10.1016/s0889-8545(05)70307-7 Gao 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 Gündoğdu 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 Guo 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 Hernández-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 Houston 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 Ifegwu 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 Jiang 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 Johnson 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 Kummer 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 Li 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 Li 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 Marquardt 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 McLeod 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 Mehta 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 Missmer 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 Moini 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 Olsson 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 Peters 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 Ramesh 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 Romanoff 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 Rowlands 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 Rumph 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 Sadeu 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 Scheurer 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 Stockinger 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 Sverdrup 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 Unwin 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 Vercellini 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 Wang 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 Zhong 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

Acknowledgements

We thank all the participants in the study. Author information Authors and Affiliations Contributions B.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. Corresponding author Ethics declarations Ethical approval NHANES Institutional Review Board approved the ethical conduct of NHANES 2003–2006. Consent to participate Every participant signed an informed consent form. Consent for publication Not applicable. Conflict of interest The authors declare no competing interests. Additional information Responsible Editor: Lotfi Aleya Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Rights and permissions Springer 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. About this article Cite this article Wang, 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 Received: Accepted: Published: Version of record: Issue date: DOI: https://doi.org/10.1007/s11356-023-30545-1

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