Environmental Exposure to Non-Persistent Endocrine Disrupting Chemicals and Endometriosis: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Selection Criteria
2.3. Study Selection
3. Results
3.1. Exposure to Phthalates and Endometriosis
3.2. Exposure to Bisphenol A and Endometriosis
3.3. Exposure to Parabens and Endometriosis
3.4. Exposure to Benzophenones and Endometriosis
3.5. Exposure to Non-Persistent Pesticides and Endometriosis
Study | Study Design | Samples Measured | Concentration of Endocrine Disrupting Chemicals (EDC) | Study Population | RESULTS | |
---|---|---|---|---|---|---|
Upson et al. (2013) [41] United States, Seattle, research was conducted among of a large healthcare system in the U.S. Pacific Northwest | population-based case-control | urinary concentration of MEHP, MEHHP, MEOHP, MECPP, MBzP, MEP, MiBP, MnBP LOQ = 0,2 ng/mL | Median (IQR): Cases: MEHP = 2.2 ng/mL (0.6–4.6) MEHHP = 14.8 ng/mL (5.3–31.0) MEOHP = 8.1 ng/mL (3.5–18.0) MECPP = 14.4 ng/mL (5.9–32.5) MBzP = 4.5 ng/mL (2.2–9.9) MEP = 61.9 ng/mL (23.5–155.9) MiBP = 1.3 ng/mL (0.6–2.7) MnBP = 9.8 ng/mL (5.0–20.9) | Median (IQR): Controls: MEHP = 3.4 ng/mL (1.0–11.1) MEHHP = 18.8 ng/mL (6.3–56.5) MEOHP = 10.8 ng/mL (3.5–29.1) MECPP = 18.0 ng/mL (5.8–51.9) MBzP = 5.0 ng/mL (2.0–11.5) MEP = 43.9 ng/mL (16.8–144.4) MiBP = 1.5 ng/mL (0.7–3.1) MnBP = 10.0 ng/mL (4.9–23.5) | 287 reproductive-age women 92- cases 195- controls Women with endometriosis age range 18–49 years Women were recruited by in-person interviews covering a range of topics, including reproductive history and contraceptive use as well as medical and family history and lifestyle behaviors. The case group was surgically-confirmed cases and population-based controls. (1996–2001) | A strong inverse association between urinary MEHP concentration and endometriosis, when comparing the fourth and first MEHP quartiles (OR 0.3, 95% CI: 0.1–0.7). No statistically significant association between urinary concentrations of other DEHP metabolites MEHHP, MEOHP, and ∑DEHP and endometriosis, increased not statistically significant of endometriosis and urinary concentrations of MBzP and MEP was found. |
Fernandez et al. (2019) [42] Brazil, Diagnosis of endometriosis was performed at the Endometriosis Center of Hospital School of the Federal University of Minas Gerais. | case-control study | urinary concentration of MMP, MiBP, MBP, MCHP, MiNP, MOP, MBzP, MEHP | Median: Cases: MMP = 57.6 µg/g MiBP = 129.8 µg/g MBP = 64.2 µg/g MCHP = 7.0 µg/g MEHP = 22.4 µg/g MiNP = 21.8 µg/g MOP = 670 µg/g MBzP = 23.8 µg/g | Median: Controls: MMP = 45.3 µg/g MiBP = 181.8 µg/g MBP = 72.4 µg/g MCHP = 4.6 µg/g MEHP = 21.2 µg/g MiNP = 14.7 µg/g MOP <LOQ MBzP < LOQ | 52 women 30—cases 22- controls Women with endometriosis age range 18–45 years Participants signed a free informed consent form and filled out a questionnaire, with questions related to food habits, gynecological history, medicine intake as well as personal information. Criteria were confirmation of endometriosis by video laparoscopy surgery with histological diagnosis and the absence of the disease, respectively. | The phthalate metabolites that had the highest concentrations, were MOP and MiBP, in which the values of 670 µg/g and 560 µg/g, respectively. The relationship between endometriosis and all grouped metabolites was not statistically significant with p = 0.225. |
Reddy et al. [43] (2006) India, The women were recruited at two centers: Bhagwan Mahavir Medical Hospital and Research Centre and Maternal Health and Reproductive Institute of Reproductive Medicine, Hyderabad, which receives cases from all over the region of Andhra Pradesh | case-control study | Serum cocncentration of DnBP, BBP, DnOP, DEHP | Arithmetic mean: Cases: DnBP = 0.44 µg/mL BBP = 0.66 µg/mL DnOP = 3.32 µg/mL DEHP = 2.44 µg/ml | Arithmetic mean: Controls I: DnBP = 0.08 µg/mL BBP = 0.12 µg/mL DnOP = 0 µg/mL DEHP = 0.5 µg/mL Controls II DnBP = 0.15 µg/mL BBP = 0.11 µg/mL DnOP = 0 µg/mL DEHP = 0.45 µg/mL | 108 reproductive-age women. 49—cases 38—controls I 21—controls II Average age was 26.6 years in endometriosis cases, 27.4 years in control group I 27.1 years in control group II. Women completed a questionnaire to obtain information on the general obstetric and gynecological details including age at menarche, length of the menstrual cycle, associated symptoms, duration and amount of blood loss, duration of infertility, and socio-demographic details like age, body mass index (BMI) and limited information on diet were used for this study. The case group included 49 women who were diagnosed with endometriosis by laparoscopy. Group I comprised 38 women who attended the same hospital for other gynecological pathology (e.g., fibroids, tubal defects, polycystic ovaries, idiopathic infertility, and pelvic inflammatory disease) but were laparoscopically without endometriosis. Control group II comprised 21 women who attended the same hospital for laparoscopic tubal sterilization, with proven fertility and no evidence of endometriosis or other gynecological disorders. | The phthalate esters were observed in all samples for women with endometriosis. Besides correlation PEs with endometriosis was strong and statistically significant at p < 0.05 for all compounds DnBP: p < 0.0001; BBP: p < 0.0001; DnOP: p < 0.0001 DEHP: p < 0.0014 |
Cobellis et al. (2003) [44] Italy No information about the centers of treatment. | case-control study | Serum concentrations or peritoneal fluid of DEHP and MEHP | Serum concentrations Cases: Median DEHP = 0.57 µg/mL MEHP = 0.38 µg/mL Peritoneal fluid Cases: Median DEHP = 0.46 µg/mL MEHP = 0.37 µg/mL | Controls: Median DEHP = 0.18 µg/mL MEHP = 0.58 µg/mL | 79 women 55—cases 24—controls Women with endometriosis age range 22–45 years. Women aged range 18–48 years without known infertility or reproductive diseases served in the controls. Diagnosis was confirmed by histological examination of the endometriotic lesions. Exclusion criteria were medical treatment for endometriosis or ovarian cyst before the surgery, and any surgical procedure in the previous 12 months. | Endometriotic women showed significantly higher plasma DEHP concentrations than controls. No significant differences in either the DEHP/MEHP plasma concentrations (p > 0.31) or DEHP/MEHP peritoneal fluid concentrations (p > 0.66) were observed in the endometriotic patients as a function of the disease stage at the time of diagnosis. |
Huang et al. (2010) [45] Taiwan Women with endometriosis came from the Department of Obstetrics and Gynecology at a medical center in Taiwan. | Case-control study | Urinary concentration of MMP, MEP, MnBP, MBzP, 5oxo-MEHP, 5OH-MEHP, MEHP, ΣMEHP | Median Cases: MMP = 37.8 ng/mL/52.4 µg/g creatinine MEP = 31.6 ng/mL/58.0 µg/g creatinine MnBP = 60.2 ng/mL/94.1 µg/g creatinine MBzP = 5.6 ng/mL/12.2 µg/g creatinine 5oxo-MEHP = 12.1 ng/mL/19.0 µg/g creatinine 5OH-MEHP = 13.6 ng/mL/16.7 µg/g creatinine MEHP = 2.7 ng/mL 4.2 µg/g creatinine ΣMEHP = 28.7 ng/mL/42.4 µg/g creatinine | Median Controls: MMP = 28.1 ng/mL/32.1 µg/g creatinine MEP = 37.2 ng/mL/71.4 µg/g creatinine MnBP = 35.4 ng/mL/58.0 µg/g creatinine MBzP = 5.9 ng/mL/8.9 µg/g creatinine 5oxo-MEHP = 9.2 ng/mL/7.8 µg/g creatinine 5OH-MEHP = 5.7 ng/mL/9.9 µg/g creatinine MEHP = 0.8 ng/mL/3.4 µg/g creatinine ΣMEHP = 28.5 ng/mL/18.9 µg/g creatinine | 57 women 28 with endometriosis 29—control group Women with endometriosis were recruited who underwent laparotomy and had pathologic confirmation of endometriosis. Controls were patients without any gynecologic conditions. (2005–2007) | In cases versus controls, an increased level of urinary mono-n-butyl phthalate (94.1 versus 58.0 µg/g creatinine, OR 3.46, Cl: 1.16–10.3, p < 0.05) was observed |
Weuve et al. (2010) [46] United States Massachusetts The women were recruited from National Health and Nutrition Examination Survey (NHANES) | cross-sectional study | Urinary concentration of MEHP, MBP, MEP, MBzP, MEHHP, MEOHP | Geoetric mean (SD) Cases: MBP = 28.9 (4.1) ng/mg MEP = 207.0 (27.5) ng/mg MEHP = 2.5 (0.4) ng/mg MBzP = 14.4 (2.5) ng/mg MEHHP = 16.5 (2.8) ng/mg MEOHP = 11.5 (1.9) ng/mg | Geoetric mean (SD) Controls: MBP = 25.5 (1.0) ng/mg MEP = 219.9 (14.1) ng/mg MEHP = 3.4 (0.1) ng/mg MBzP = 14.1 (0.6) ng/mg MEHHP = 19.7 (1.4) ng/mg MEOHP = 13.5 (1.0) ng/mg | 1227 women 87 with endometriosis 1020 control group Women was recruited 20–54 years of age. Sociodemographic information and medical histories of the survey participants and their families were collected during the household interviews Women were classified based on the history of endometriosis according to their response to the question “Has a doctor or other health professional ever told you that you had endometriosis?” (1999–2004) | No statistically significant association between assessed metabolites and endometriosis was found. |
Nair et al. (2018) [47] Pakistan/ Australia This study was financially supported by the University of Health Sciences, Lahore, Pakistan. | case-control study | Serum concentration of DEHP | Arithmetic mean: Cases: DEHP = 65.29 (ng/mL) Arithmetic mean in all the four stages of endometriosis: DEHP stage I = 60.4 ng/mL DEHP stage II = 58.68 ng/mL DEHP stage III = 66.25 ng/mL DEHP stage IV = 68.11 ng/mL | Arithmetic mean: Controls: Not detected | 100 women 50 with endometriosis 50 without endometriosis Women with endometriosis age range 20–40 years. Only cases were included who were infertile and had been declared positive for endometriosis after laparoscopy by expert surgeons, according to the criteria set by the American Society for Reproductive Medicine (ASRM, 2012). ASRM guidelines classify endometriosis into four stages: I—minimal, II—mild, III—moderate, and IV—severe. For controls, due to ethical considerations, laparoscopy was not done. | DEHP exposure was associated with advanced stages III and IV of endometriosis. |
Louis et al. (2013) [48] United States, Utah The women were recruited in 14 participating clinical centers in the Salt Lake City, Utah, and San Francisco, California geographic areas. | matched cohort design | Urinary concentration of phthalate metabolites: MMP, MEP, MCPP, MBP, MiBP, MECPP, MCMHP, MEHHP, MEOHP, MCHP, MBzP, MEHP | Geometric mean Operative Cohort: Endometriosis: MMP = 2.12 ng/mL MEP = 107.2 ng/mL MCPP = 2.71 ng/mL MBP = 12.07 ng/mL MiBP = 7.28 ng/mL MECPP = 24.68 ng/mL MCMHP = 29.34 ng/mL MEHHP = 16.34 ng/mL MEOHP = 10.98 ng/mL MCHP = 0.03 ng/mL MBzP = 6.96 ng/mL MEHP = 4.75 ng/mL MOP = 0.06 ng/mL MNP = 0.16 ng/mL Without endometriosis: MMP = 2.35 ng/mL MEP = 109.6 ng/mL MCPP = 3.41 ng/mL MBP = 11.01 ng/mL MiBP = 6.82 ng/mL MECPP = 24.98 ng/mL MCMHP = 29.19 ng/mL MEHHP = 14.40 ng/mL MEOHP = 10.12 ng/mL MCHP = 0.04 ng/mL MBzP = 7.82 ng/mL MEHP = 4.12 ng/mL MOP = 0.06 ng/mL MNP = 0.16 ng/mL | Geometric mean Population Cohort Endometriosis: MMP = 3.67 ng/mL MEP = 152.0 ng/mL MCPP = 5.75 ng/mL MBP = 19.13 ng/mL MiBP = 13.32 ng/mL MECPP = 54.15 ng/mL MCMHP = 53.54 ng/mL MEHHP = 32.37 ng/mL MEOHP = 23.03 ng/mL MCHP = 0.04 ng/mL MBzP = 9.85 ng/mL MEHP = 8.32 ng/mL MOP = 0.06 ng/mL MNP = 0.22 ng/mL Without endometriosis: MMP = 2.71 ng/mL MEP = 138.2 ng/mL MCPP = 4.06 ng/mL MBP = 11.24 ng/mL MiBP = 7.59 ng/mL MECPP = 20.27 ng/mL MCMHP = 22.51 ng/mL MEHHP = 11.86 ng/mL MEOHP = 8.29 ng/mL MCHP = 0.03 ng/mL MBzP = 6.46 ng/mL MEHP = 3.07 ng/mL MOP = 0.05 ng/mL MNP = 0.16 ng/mL | 626 women 495 operative cohort 131 population cohort Women was recruited 18–44 years of age. In-person standardized interviews were conducted with women prior to surgery or MRI followed by an anthropometric assessment Operative cohort was undergoing laparoscopy/laparotomy. Endometriosis was confirmed in 190 women, and 283 were without endometriosis. The population cohort received standardized pelvic magnetic resonance imaging (MRI) for the assessment of endometriosis. 127 women were confirmed with endometriosis in the population cohort. (2007–2009) | A significant association was observed between MBP, MCMHP, MECPP, MEHP, MEHHP, and MEOHP and endometriosis in the population cohort. No significant association between urinary concentration phthalates occurrence and endometriosis in the operative cohort. |
Itoh et al. (2009) [49] Japan The women were recruited from the Department of Obstetrics and Gynecology of the Jikei University School of Medicine for the treatment of infertility. | case-control study | Urinary concentration of MEP, MnBP, MBzP, MEHP, MEHHP, MEOHP | Cases (II-IV stages): Median unadjusted for creatinine (creatinine-adjusted) MEP = 39.6 µg/L (18.9 µg/g creatinine) MnBP = 87.2 µg/L (47.6 µg/g creatinine) MBzP = 3.9 µg/L (2.1 µg/g creatinine) MEHP = 10.2 µg/L (4.9 µg/g creatinine) MEHHP = 39.6 µg/L (19.2 µg/g creatinine) MEOHP = 39.5 µg/L (19.1 µg/g creatinine) | Controls (0–1 stages): Median unadjusted for creatinine (creatinine-adjusted) MEP = 21.4 µg/L (11.2 µg/g creatinine) MnBP = 84.3 µg/L (43.3 µg/g creatinine) MBzP = 3.2 µg/L (1.8 µg/g creatinine) MEHP = 8.3 µg/L (4.2 µg/g creatinine) MEHHP = 32.2 µg/L (17.3 µg/g creatinine) MEOHP = 32.1 µg/L (16.3 µg/g creatinine) | 137 women Women were recruited 20–45 years of age. Participants were interviewed before laparoscopic examination by a single trained interviewer using a structured questionnaire to collect information on demographic factors, age, height, weight, personal and family medical, reproductive and menstrual history, oral contraceptive use, food, and alcohol consumption, and smoking history. The severity of endometriosis was diagnosed using laparoscopy. Cases of endometriosis have been classified into five stages based on the American Fertility Society classification and then categorized into: 80 controls (stage 0 or I) 57 cases (stages II-IV). (I-minimal, II-mild, III-moderate, and IV-severe) | No significant association between endometriosis and urinary concentration of phthalate. |
Kim et al. (2015) [50] Korea The women were recruited from the department of Obstetrics & Gynecology in Asan Medical Center, Seoul, Korea. | case-control study | Urinary concentration of: MEHHP, MEOHP, MnBP, MECPP | Arithmetic mean ± SE Cases: MEHHP = 18.2 ± 1.7 µg/g creatinine MEOHP = 13.4 ± 1.1 µg/g creatinine MnBP = 41.7 ± 6.2 µg/g creatinine MBzP = 5.8 ± 1.0 µg/g creatinine MECPP = 23.8 ± 1.9 µg/g creatinine | Arithmetic mean ± SE Controls: MEHHP = 12.9 ± 1.4 µg/g creatinine MEOHP = 10.3 ± 0.9 µg/g creatinine MnBP = 32.4 ± 3.1 µg/g creatinine MBzP = 7.3 ± 1.9 µg/g creatinine MECPP = 19.0 ± 1.7 µg/g creatinine | 88 women 55—cases 33—controls The mean age in the endometriosis group was 29.9 years and in the control group was 32.6 years. Any women with a history of occupational exposure to reproductive toxicants, smoking, alcohol, and other addictions were excluded from this study. Th endometriosis group had undergone pelviscopic surgery, exploratory laparotomy, or transabdominal hysterectomy. (2012–2013) | Significant association between urinary concentrations of phthalates and endometriosis: MEHHP OR = 2.52; p = 0.041 MEOHP OR = 2.89; p = 0.043 MECPP OR = 2.57; p = 0.071 |
Kim et al. (2011) [51] Korea The women were recruited from the department of Obstetrics and Gynecology in Asan Medical Center, Seoul, Korea | case-control study | Serum concentration of MEHP, DEHP | Arithmetic mean ± SE Cases: MEHP = 17.4 ± 1.5 ng/mL DEHP = 179.7 ± 32.5 ng/mL | Arithmetic mean ± SE Controls: MEHP = 12.4 ± 1.1 ng/mL DEHP = 92.5 ± 31.1 ng/mL | 266 women 97—cases 169—controls All of the subjects recruited in this study were from urban areas, without a history of occupational exposure to reproductive toxicants, smoking, alcohol, and other addictions. This study comprised a total of 266 patients who had undergone pelviscopic surgery, exploratory laparotomy, myomectomy, or transabdominal hysterectomy. The endometriosis group had surgical and histologic evidence of advanced-stage endometriosis. (January 2009 and September 2009. | Plasma levels of MEHP were significantly higher in those with advanced-stage of endometriosis (levels of phthalate esters might be quite different between the patients with stage I–II and III–IV endometriosis). MEHP OR = 1.020(1.003–1.038)/p = 0.020 No significant association between DEHP and endometriosis. DEHP OR= 1.001 (1.000–1.002)/p = 0.161 |
Zhang et al. (2021) [52] China The women were recruited from the National Health and Nutrition Examination Survey (NHANES) | cross-sectional study | Urinary concentration of: MBP, MCHP, MEP, MEHP, MNP, MOP, MBzP, MNM, MCPP, MEHHP, MEOHP, MIBP | Geometric mean for the whole population: MBP = 20.89 ng/mL MCHP = 0.45 ng/mL MEP = 160.27 ng/mL MEHP = 3.55 ng/mL MNP = 1.19 ng/mL MOP = 1.32 ng/mL MBzP = 8.80 ng/mL MNM = 1.65 ng/mL MCPP = 2.16 ng/mL MEHHP = 20.06 ng/mL MEOHP = 14.03 ng/mL MIBP = 4.13 ng/mL | 1204 women 77—cases 1127—controls Women were recruited from 20–54 years of age, information about endometriosis was based on a questionnaire. (2001–2006) | No association between examined phthalates metabolites and endometriosis. |
Study | Study Design | Samples Measured | Concentration of Endocrine Disrupting Chemicals (EDC) | Study Population | Results | |
---|---|---|---|---|---|---|
Fernandez et al. (2019) [42] Brazil Diagnosis of endometriosis was performed at the Endometriosis Center of Hospital School of the Federal University of Minas Gerais. | case-control study | Urinary concentration of BPA | Median Cases: BPA = 8.9 µg/g | Median: Controls: BPA = 8.8 µg/g | 52 women 30—cases 22—controls Women with endometriosis age range 18–45 years Participants signed a free informed consent form and filled out a questionnaire, with questions related to food habits, gynecological history, medicine intake as well as personal information. Criteria were confirmation of endometriosis by video laparoscopy surgery with histological diagnosis and the absence of the disease, respectively. | No association between BPA in the urine and endometriosis. |
Itoh et al. (2007) [66] Japan Women were recruited from the Department of Obstetrics and Gynecology of the Jikei University School of Medicine for the treatment of infertility | cross-sectional study | Urinary concentration of BPA | Median BPA = 1.57 µg/L (0.8 µg/g creatine) | 140 women The women with endometriosis age range 20–45 years. Interviews using a questionnaire to collect information on demographic factors, age, height, weight, personal and family medical, reproductive and menstrual histories, oral contraceptive use, food, and alcohol consumption frequencies, and smoking history. The endometriosis was diagnosed using laparoscopy and then classified into five stages on the basis of the revised American Fertility Society classification: stage 0 (n = 60), I (n = 21), II (n = 10), III (n = 24), and IV (n = 25). | No association between urinary BPA concentration and endometriosis, p = 0.24 | |
Upson et al. (2014) [60] United States The women were recruited from Group Health (GH), a large integrated healthcare system in the US Pacific Northwest | case-control study | Urinary concentration of BPA | Percentage of cases with different quartiles of exposure to BPA Cases: Quartiles ≤0.364 = 21.7% >0.364–0.863 = 23.1% >0.863–2.01 = 28.0% >2.01 = 27.3% Ovarian endometriosis Cases: ≤0.364 = 29.3% >0.364–0.863 = 14.7% >0.863–2.01 = 24.0% >2.01 = 32.0% Non-ovarian pelvic endometriosis ≤0.364 = 13.2% >0.364–0.863 = 32.4% >0.863–2.01 = 32.4% >2.01 = 22.1% | Percentage of cases with different quartiles of exposure to BPA Controls: Quartiles ≤0.364 = 25.1% >0.364–0.863 = 25.1% >0.863–2.01 = 25.1% >2.01 = 24.7% | 430 women 143—cases 287—controls The women with endometriosis age range 18–49 years. In-person interview that occurred after case diagnosis, eliciting detailed reproductive, contraceptive, medical, and family history as well as lifestyle behavior information. Cases were women first diagnosed with endometriosis, with medical record confirmation of direct surgical visualization of endometriosis, and also cases had pathology-confirmed endometriosis. Controls were women identified from computerized GH enrollment databases, without a current or prior diagnosis of endometriosis. (1996–2001) | A statistically significant association between total urinary BPA concentrations and endometriosis overall. Statistically significant positive associations when evaluating total urinary BPA concentrations in relation to non-ovarian pelvic endometriosis (second versus lowest quartile: OR 3.0; 95% CI: 1.2, 7.3; third versus lowest quartile: OR 3.0; 95% CI: 1.1, 7.6), but not in relation to ovarian endometriosis |
Peinado et al. (2020) [61] Spain The women were recruited from the Surgery and the Gynecology and Obstetrics Units of the San Cecilio and Virgen de las Nieves University Hospitals in Granada, southern Spain | case-control study | Urinary concentrations of BPA | Geometric mean ± SD Cases: BPA = 5.5 (1.1) ng/mL | Geometric mean ± SD Controls: BPA = 3.0 (1.2) ng/mL | 124 women 35—case 89—control The women with endometriosis age range 20–54 years. Women underwent clinical and anthropometrical examination, calculating their BMI from their height and weight. Surgical and clinical questionnaires were used to gather sociodemographic, lifestyle, clinical, and surgical data, including residence, educational level, occupational status, current smoking, parity, and the average level of menstrual bleeding. Cases were women with endometriosis diagnosed by laparotomy or laparoscopic surgery and histological confirmation, while controls were women undergoing abdominal surgery for non-malign diseases (including acute appendicitis, biliary disease, hiatus hernia, ovarian torsion, corpus luteum, uterine fibroids, and cystadenomas, among others) in whom the absence of endometrial lesions was visually and histologically confirmed. (2018–2019) | Association between BPA concentrations and endometriosis OR = 1.5; p < 0.05 |
Rashidi et al. (2017) [62] Iran This case-control study was approved by the Institutional Review Board of Tehran University of Medical Sciences. The samples were analyzed at Pharmaceutical Science Research Center of Tehran University of Medical Sciences | case-control study | Urinary concentrations of BPA | Geometric mean ± SD Cases: BPA = 5.53 ± 3.46 ng/mL | Geometric mean ± SD Controls: BPA = 1.42 ± 1.56 ng/mL | 100 women 50—case 50—control The women with endometriosis age range 22–45 years. Women filled out a questionnaire about lifestyle. Women with endometriosis were candidates for operative laparoscopy and ovarian cystectomy as cases. Control group was women who had not any evidence of endometrioma in clinical and ultrasound evaluation and came to the same clinic. | Association between the BPA urinary concentrations among women with endometrioma were statistically higher compared with the control group. Crude OR 1.75; p < 0.001 |
Louis et al. (2013) [48] United States Utah The women were recruited in 14 participating clinical centers in the Salt Lake City, Utah, and San Francisco, California geographic areas. | matched cohort design | Urinary concentration of BPA | Geometric mean Operative Cohort: Endometriosis: BPA = 1.45 mg/dL Without endometriosis: BPA = 1.66 mg/dL | Geometric mean Population Cohort: Endometriosis: BPA = 4.19 mg/dL Without endometriosis: BPA = 1.65 mg/dL | 626 women 495 operative cohort 131 population cohort Women were recruited 18–44 years of age. In-person standardized interviews were conducted with women prior to surgery or MRI followed by an anthropometric assessment Operative cohort was undergoing laparoscopy/laparotomy. Endometriosis was confirmed in 190 women, and 283 were without endometriosis. The population cohort had standardized pelvic magnetic resonance imaging (MRI) for the assessment of endometriosis. 127 women were confirmed with endometriosis in the population cohort. (2007–2009) | No association between BPA concentration and endometriosis in the operative cohort and population cohort. |
Simonelli et al. (2016) [63] Italy Women with endometriosis and endometriosis-free subjects were referred to the outpatient infertility clinic at the Second University of Naples. | case-control study | Urinary concentration of BPA | Arithmetic mean Endometriosis: BPA = 5.31 ± 3.36 pg/µl | Arithmetic mean Control: BPA = 1.64 ± 0.49 pg/µl | 128 women 68—case 60—control The age of the group was not provided in the study, the author included age ranges (x < 30; 30 ≤ x ≥ 35; 35 ≤ x ≥ 40; x ≥ 40). A questionnaire investigating the occupational context, living environment, and habits was administered to patients suffering from endometriosis and endometriosis-free subjects (control group). All women with a regular menstrual cycle undergoing laparoscopy because of infertility, chronic pelvic pain, or sonographic diagnosis of ovarian endometriosis were recruited. Laparoscopy was performed in the proliferative phase, evidenced by hormone and ultrasonography (USG) analyses. Sixty-eight women were diagnosed with a histologically confirmed diagnosis of endometriosis; 60 women were control group. | A statistically significant difference between patients and controls, showing an association between BPA exposure and endometriosis. |
Cobellis et al. (2009) [64] Italy The study was approved by the institutional review board of the Second University of Naples; informed consent was obtained from the participants. A group of fertile women referred to the Department of Gynaecology, Obstetrics, and Reproductive Medicine of the same university was enrolled. | case-control study | Serum concentration of BPA | Arithmetic mean ± SD Cases: BPA = 2.91 ± 1.74 ng/mL | Arithmetic mean: Controls: Not detected | 69 women 58—cases 11—controls The women with endometriosis age range 18–44 years. No information about lifestyle from a questionnaire. The patients were submitted to diagnostic or operative laparoscopy for the evidence of ovarian cysts or to investigate chronic pelvic pain and dysmenorrhea The endometriosis diagnosis was confirmed by histological examination of the endometriotic lesions, and patients were classified according to the revised American Fertility Society classification of endometriosis. | BPA has not been found in any of the between from healthy women (control group). However, BPA has been observed in 30 women with endometriosis. |
Wen et al. (2020) [65] China The women were recruited from the Obstetrics and Gynecology Department of Zhongnan Hospital, Wuhan University. A control group with another 100 cases of healthy women who sought help because of their husband’s infertility in the Reproductive Medicine Center or who had a routine physical examination in the Medical Examination Center of Zhongnan Hospital, Wuhan University, were also recruited as the control group. | case-control study | Urinary concentration of BPA | Median (IQR) Cases: BPA = 1.55 (0.85–1.95) µg/g | Median (IQR) Controls: BPA = 1.30 (0.74–1.99) µg/g | 220 women 120—cases 100—controls Women were recruited 20–50 years of age. Women completed a questionnaire about lifestyle. Women undergoing laparoscopy were defined as EMs histopathologically. Patients with ovarian EMs who displayed peritoneal lesions were excluded from this study. Finally, 120 patients (including 73 cases of ovarian EMs, 47 cases of peritoneal EMs) were recruited as the case group. In this study, controls were women who met the following three conditions: aged from 20 to 50 years; without a current or prior diagnosis of EMs or infertility; and had no ovarian or other pelvic, abdominal masses suggested by B-ultrasound. All subjects were in the proliferative phase of the menstrual cycle determined by their menstrual history and were free of any hormone treatment for > 3 months prior to sample collection. Other gynecologic diseases such as adenomyosis, hysteromyoma, endometrial polyp, and polycystic ovary syndrome were also excluded. (2017–2018) | Association between the BPA urinary concentrations among women with endometrioma were higher compared with the control group. The risk of peritoneal EMs increased approximately tenfold when creatinine-adjusted urinary BPA concentration was 2 μg/g. |
Study | Study Design | Samples Measured | Concentration of Endocrine Disrupting Chemicals (EDC) | Study Population | Results | |
---|---|---|---|---|---|---|
Peinado et al. (2020) [72] Spain The women with endometriosis was part of the hospital-based case-control EndEA study (Endometriosis y Exposicion Ambiental), in two public hospitals (‘San Cecilio’ and ‘Virgen de las Nieves’) in Granada, Southern Spain | case-control study | Urinary concentration of MeP, EtP, PrP, BuP | Arithmetic mean ± SD Cases: MeP = 210.98 ± 512.79 ng/mL EtP = 35.18 ± 79.27 ng/mL PrP = 14.35 ± 30.22 ng/mL BuP = 1.15 ± 3.42 ng/mL | Arithmetic mean ± SD Controls: MeP = 148.91 ± 272.94 ng/mL EtP = 37.12 ± 118.82 ng/mL PrP = 8.59 ± 18.87 ng/mL BuP = 1.40 ± 2.25 ng/mL | 124 women 35—case 89—control The women with endometriosis age range 20–54 years. The women filled out a questionnaire about lifestyle and used cosmetics products. Endometriosis was confirmed (cases) or ruled out (controls) by laparoscopy, with a visual inspection of the pelvis and biopsy of suspected lesions (histological diagnosis) Inclusion criteria were: receipt of abdominal surgery (laparotomy or laparoscopy) and pathology report on the presence or absence of endometriosis. Further criteria for controls were: performance of laparotomy or laparoscopy in the same hospital as cases for non-malignant disease (e.g., acute appendicitis, biliary disease, hiatus hernia, ovarian torsion, corpus luteum, and cystadenomas, among others), no findings of endometriosis during the surgery, and no history of endometriosis. (2018–2019) | Significant association between endometriosis and urinary concentration of MeP (OR 5.63, p < 0.001). No association with others examined parabens and endometriosis. |
Study | Study Design | Samples Measured | Concentration of Endocrine Disrupting Chemicals (EDC) | Study Population | Results | |
---|---|---|---|---|---|---|
Peinado et al. (2020) [72] Spain The women with endometriosis were, part of the hospital-based case-control EndEA study (Endometriosis y Exposicion Ambiental), in two public hospitals (‘San Cecilio’ and ‘Virgen de las Nieves’) in Granada, Southern Spain | case-control study | Urinary concentration of BP-1, BP-3, 4-OH-BP | Arithmetic mean ± SD Case: BP-1 = 3.37 ± 4.99 ng/mL BP-3 = 10.84 ± 32.61 ng/mL 4-OH-BP = 0.99 ± 1.01 ng/mL | Arithmetic mean ± SD Control: BP-1 = 22.73 ± 107.95 ng/mL BP-3 = 35.07 ± 115.36 ng/mL 4-OH-BP = 3.26 ± 19.61 ng/mL | 124 women 35—case 89—control The women with endometriosis age range 20–54 years. The women filled out a questionnaire about lifestyle and used cosmetics products. Endometriosis was confirmed (cases) or ruled out (controls) by laparoscopy, with a visual inspection of the pelvis and biopsy of suspected lesions (histological diagnosis) Inclusion criteria were: receipt of abdominal surgery (laparotomy or laparoscopy), and pathology report on the presence or absence of endometriosis. Further criteria for controls were: performance of laparotomy or laparoscopy in the same hospital as cases for non-malignant disease (e.g., acute appendicitis, biliary disease, hiatus hernia, ovarian torsion, corpus luteum, and cystadenomas, among others), no findings of endometriosis during the surgery, and no history of endometriosis. (2018–2019) | Significant association between endometriosis and urinary concentration of BP-1 (OR = 5.12, p = 0.011) and BP-3 (OR = 4.98, p = 0.008). Others benzophenones have not been associated with endometriosis. |
Kunisue et al. (2012) [76] United States Utah and California Urine samples were collected for the ENDO (Endometriosis, Natural history, Diagnosis, and Outcomes) from women who resided within 50 miles of two cities, Salt Lake City (Utah) and San Francisco (California) | matched cohort study | Urinary concentration of 2OH-4MeO-BP, 2,4OH-BP, 4OH-BP | Median for the study cohort sum 2OH-4MeO-BP = 6.1 ng/mL 2,4OH-BP = 6.1 ng/mL 4OH-BP = 0.36 ng/mL | 600 women 473—operative cohort 127—population cohort The women with endometriosis age range 18–44 years. The women filled out a questionnaire about lifestyle The women underwent laparoscopy/laparotomy (operative cohort) or pelvic magnetic resonance imaging (population cohort). Endometriosis diagnoses were categorized into four stages: minimal, mild, moderate, and severe according to the Revised American Society for Reproductive Medicine’s classification. (2007–2009) | No association between urinary concentration and benzophenone-type UV Filters and endometriosis. Operative cohort: 2OH-4MeO-BP, OR = 1.08, 2,4OH-BP, OR = 1.19, 4OH-BP, OR = 0.97, Population cohort: 2OH-4MeO-BP, OR = 1.25, 2,4OH-BP, OR = 1.03, 4OH-BP, OR = 1.19, |
Study | Study Design | Samples Measured | Concentration of Endocrine Disrupting Chemicals (EDC) | Study Population | Results |
---|---|---|---|---|---|
Li et al. (2020) [87] United States Utah and California Urine samples were collected for the ENDO (Endometriosis, Natural history, Diagnosis, and Outcomes) from women who resided within 50 miles of two cities, Salt Lake City (Utah) and San Francisco (California) | matched cohort study | Urinary concentration of IMPY, MDA, PNP, TCPY, 2,4-D, 2,4,5-T, 3-PBA, 4F-3PBA, trans-DCCA, cis-DCCA, cis-DBCA | Median for the study cohort sum IMPY = 2.70 ng/mL MDA = 0.217 ng/mL PNP = 0.637 ng/mL TCPY = 0.601 ng/mL 2,4-D = 0.249 ng/mL 2,4,5-T < LOD 3-PBA = 0.166 ng/mL 4F-3PBA = 0.008 ng/mL trans-DCCA = 0.055 ng/mL cis-DCCA = 0.091 ng/mL cis-DBCA < LOD | 594 women 471—operative cohort 123—population cohort The women with endometriosis age range 18–44 years. The women filled out a questionnaire about lifestyle The women underwent laparoscopy/laparotomy (operative cohort) or pelvic magnetic resonance imaging (population cohort). Endometriosis diagnoses were categorized into four stages: minimal, mild, moderate, and severe, according to the Revised American Society for Reproductive Medicine’s classification. (2007–2009) | A significant association between endometriosis and urinary concentration of diazinon (the parent compound of IMPY) and chlorpyrifos and chlorpyrifos-methyl (parent compounds of TCPY) IMPY, OR = 1.89 TCPY, OR = 1.65 |
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Eskenazi, B.; Warner, M.L. Epidemiology of endometriosis. Obstet. Gynecol. Clin. North Am. 1997, 24, 235–258. [Google Scholar] [CrossRef]
- Houston, D.E. Evidence for the risk of pelvic endometriosis by age, race and socioeconomic status. Epidemiol. Rev. 1984, 6, 167–191. [Google Scholar] [CrossRef] [PubMed]
- Giudice, L.C.; Kao, L.C. Endometriosis. Lancet 2004, 364, 1789–1799. [Google Scholar] [CrossRef]
- Dunselman, G.A.J.; Vermeulen, N.; Becker, C.; Calhaz-Jorge, C.; D’Hooghe, T.; De Bie, B.; Heikinheimo, O.; Horne, A.W.; Kiesel, L.; Nap, A.; et al. ESHRE guideline: Management of women with endometriosis. Hum. Reprod. 2014, 29, 400–412. [Google Scholar] [CrossRef] [PubMed]
- Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: A committee opinion. Fertil. Steril. 2012, 98, 591–598. [Google Scholar] [CrossRef] [PubMed]
- Taf, S. Classification of endometriosis. The American Fertility Society. Fertil. Steril. 1979, 6, 633–634. [Google Scholar]
- Nisolle, M.; Donnez, J. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil. Steril. 1997, 68, 585–596. [Google Scholar] [CrossRef]
- Symons, L.K.; Miller, J.E.; Kay, V.R.; Marks, R.M.; Liblik, K.; Koti, M.; Tayade, C. The Immunopathophysiology of Endometriosis. Trends Mol. Med. 2018, 24, 748–762. [Google Scholar] [CrossRef]
- Cramer, D.W.; Missmer, S.A. The epidemiology of endometriosis. Ann. N. Y. Acad. Sci. 2002, 955, 11–22. [Google Scholar] [CrossRef]
- Missmer, S.A.; Hankinson, S.E.; Spiegelman, D.; Barbieri, R.L.; Marshall, L.M.; Hunter, D.J. Incidence of Laparoscopically Confirmed Endometriosis by Demographic, Anthropometric, and Lifestyle Factors. Am. J. Epidemiol. 2004, 160, 784–796. [Google Scholar] [CrossRef]
- Crain, N.; Jansen, N.; Edwads, T. Female reproductive disorders: The roles of endocrine-disrupting compounds and developmental timing. Fertil. Steril. 2008, 90, 911–940. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pauwels, A.; Schepens, P.J.C.; D’Hooghe, T.; Delbeke, L.; Dhont, M.; Brouwer, A.; Weyler, J. The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: A case–control study of infertile women. Hum. Reprod. 2001, 16, 2050–2055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eskenazi, B.; Mocarelli, P.; Warner, M.; Samuels, S.; Vercellini, P.; Olive, D.; Needham, L.L.; Patterson, D.G., Jr.; Brambilla, P.; Gavoni, N.; et al. Serum dioxin concentrations and endometriosis: A cohort study in Seveso, Italy. Environ. Health Perspect. 2002, 110, 629–634. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yao, M.; Hu, T.; Wang, Y.; Du, Y.; Hu Ch Wu, R. Polychlorinated biphenyls and its potential role in endometriosis. Environ. Pollut. 2017, 229, 837–845. [Google Scholar] [CrossRef]
- Niskar, A.S.; Needham, L.L.; Rubin, C.; Turner, W.E.; Martin, C.A.; Patterson, D.G.; Hasty, L.; Wong, L.-Y.; Marcus, M. Serum dioxins, polychlorinated biphenyls, and endometriosis: A case-control study in Atlanta. Chemosphere 2009, 74, 944–949. [Google Scholar] [CrossRef]
- Trabert, B.; De Roos, A.J.; Schwartz, S.M.; Peters, U.; Scholes, D.; Barr, D.B.; Holt, V.L. Non-dioxin-like polychlorinated biphenyls and risk of endometriosis. Environ. Health Perspect. 2010, 118, 1280–1285. [Google Scholar] [CrossRef] [Green Version]
- Upson, K.; De Roos, A.J.; Thompson, M.L.; Sathyanarayana, S.; Scholes, D.; Barr, D.B.; Holt, V.L. Organochlorine pesticides and risk of endometriosis: Findings from a population-based case-control study. Environ. Health Perspect. 2013, 121, 1319–1324. [Google Scholar] [CrossRef] [Green Version]
- Lebel, G.; Dodin, S.; Ayotte, P.; Marcoux, S.; Ferron, L.A.; Dewailly, E. Organochlorine exposure and the risk of endometriosis. Fertil. Steril. 1998, 69, 221–228. [Google Scholar] [CrossRef]
- Cooney, M.A.; Louis, G.M.; Buck Hediger, M.L.; Vexler, A.; Kostyniak, P.J. Organochlorine pesticides and endometriosis. Reprod. Toxicol. 2010, 30, 365–369. [Google Scholar] [CrossRef] [Green Version]
- Diamanti-Kandarakis, E.; Bourguignon, J.-P.; Giudice, L.C.; Hauser, R.; Prins, G.S.; Soto, A.M.; RZoeller, T.; Gore, A.C. Endocrine-Disrupting Chemicals: An Endocrine Society Scientific Statement. Endocr. Rev. 2009, 30, 293–342. [Google Scholar] [CrossRef]
- Jurewicz, J.; Hanke, W.; Radwan, M.; Bonde, J.P. Environmental factors and semen quality. Int. J. Occup. Med. Environ. Health 2009, 22, 305–329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jurewicz, J.; Radwan, M.; Sobala, W.; Ligocka, D.; Radwan, P.; Bochenek, M.; Hawuła, W.; Jakubowski, L.; Hanke, W. Human urinary phthalate metabolites level and main semen parameters, sperm chromatin structure, sperm aneuploidy and reproductive hormones. Reprod. Toxicol. 2013, 42, 232–241. [Google Scholar] [CrossRef] [PubMed]
- Vagi, S.J.; Azziz-Baumgartner, E.; Sjödin, A.; Calafat, A.M.; Dumesic, D.; Gonzalez, L.; Azziz, R. Exploring the potential association between brominated diphenyl ethers, polychlorinated biphenyls, organochlorine pesticides, perfluorinated compounds, phthalates, and bisphenol a in polycystic ovary syndrome: A case–control study. BMC Endocr. Disord. 2014, 14, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lovekamp-Swan, T.; Davis, B.J. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ. Health Perspect. 2003, 111, 139–145. [Google Scholar] [CrossRef] [Green Version]
- Jurewicz, J.; Majewska, J.; Berg, A.; Owczarek, K.; Zajdel, R.; Kaleta, D.; Wasik, A.; Rachoń, D. Serum bisphenol A analogues in women diagnosed with the polycystic ovary syndrome—Is there an association? Environ Pollut. 2021, 272, 115962. [Google Scholar] [CrossRef]
- Jurewicz, J.; Wielgomas, B.; Radwan, M.; Karwacka, A.; Klimowska, A.; Dziewirska, E.; Korczak, K.; Zajdel, R.; Radwan, P.; Hanke, W. Triclosan exposure and ovarian reserve. Reprod. Toxicol. 2019, 89, 168–172. [Google Scholar] [CrossRef]
- Hauser, R.; Duty, S.; Godfrey-Bailey, L.; Calafat, A.M. Medications as a source of human exposure to phthalates. Environ. Health Perspect. 2004, 112, 751–753. [Google Scholar] [CrossRef] [Green Version]
- Duty, S.M.; Calafat, A.M.; Silva, M.J.; Ryan, L.; Hauser, R. Phthalate exposure and reproductive hormones in adult men. Hum. Reprod. 2005, 20, 604–610. [Google Scholar] [CrossRef] [Green Version]
- Schecter, A.; Lorber, M.; Guo, Y.; Wu, Q.; Yun, S.H.; Kannan, K.; Hommel, M.; Imran, N.; Hynan, L.S.; Cheng, D.; et al. Phthalate concentrations and dietary exposure from food purchased in New York State. Env. Health Perspect. 2013, 121, 473–479. [Google Scholar] [CrossRef] [Green Version]
- Liang, Y.; Xu, Y. Emission of phthalates and phthalate alternatives from vinyl flooring and crib mattress covers: The influence of temperature. Environ. Sci. Technol. 2014, 48, 14228–14237. [Google Scholar] [CrossRef]
- Adibi, J.J.; Perera, F.P.; Jedrychowski, W.; Camann, D.E.; Barr, D.; Jacek, R.; Whyatt, R.M. Prenatal exposures to phthalates among women in New York City and Krakow, Poland. Environ. Health Perspect. 2003, 111, 1719–1722. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clark, K.E.; David, R.M.; Guinn, R.; Kramarz, K.W.; Lampi, M.A.; Staples, C.A. Modeling human exposure to phthalate esters: A comparison of indirect and biomonitoring estimation methods. Hum. Ecol. Risk Assess. Inter. J. 2011, 17, 923–965. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bornehag, C.G.; Sundell, J.; Weschler, C.J.; Sigsgaard, T.; Lundgren, B.; Hasselgren, M.; Hägerhed-Engman, L. The association between asthma and allergic symptoms in children and phthalates in house dust: A nested case–control study. Environ. Health Perspect. 2004, 112, 1393–1397. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kimber, I.; Dearman, R.J. An assessment of the ability of phthalates to influence immune and allergic responses. Toxicology 2010, 271, 73–82. [Google Scholar] [CrossRef]
- Romani, F.; Tropea, A.; Scarinci, E.; Federico, A.; Russo, C.D.; Lisi, L.; Catino, S.; Lanzone, A.; Apa, R. Endocrine disruptors and human reproductive failure: The in vitro effect of phthalates on human luteal cells. Fertil. Steril. 2014, 102, 831–837. [Google Scholar] [CrossRef]
- Chen, C.-H.; Jiang, S.S.; Chang, I.-S.; Wen, H.-J.; Sun, C.-W.; Wang, S.-L. Association between fetal exposure to phthalate endocrine disruptor and genome-wide DNA methylation at birth. Environ. Res. 2018, 162, 261–270. [Google Scholar] [CrossRef]
- Duty, S.M.; Ackerman, R.M.; Calafat, A.M.; Hauser, R. Personal care product use predicts urinary concentrations of some phthalate monoesters. Environ. Health Perspect. 2005, 113, 1530–1535. [Google Scholar] [CrossRef] [Green Version]
- Jurewicz, J.; Hanke, W. Exposure to phthalates: Reproductive outcome and children health. A review of epidemiological studies. Int. J. Occup. Med. Environ. Health 2011, 24, 115–141. [Google Scholar] [CrossRef]
- Hannon, P.R.; Flaws, J.A. The effects of phthalates on the ovary. Front. Endocrinol. 2015, 6, 8. [Google Scholar] [CrossRef]
- Hoppin, J.A.; Brock, J.W.; Davis, B.J.; Baird, D.D. Reproducibility of urinary phthalate metabolites in first morning urine samples. Environ. Health Perspect. 2002, 110, 515–518. [Google Scholar] [CrossRef] [Green Version]
- Upson, K.; Sathyanarayana, S.; De Roos, A.J.; Thompson, M.L.; Scholes, D.; Dills, R.; Holt, V.L. Phthalates and risk of endometriosis. Environ. Res. 2013, 126, 91–97. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernandez, M.A.M.; Cardeal, Z.L.; Carneiro, M.M.; André, L. Study of possible association between endometriosis and phthalate and bisphenol A by biomarkers analysis. J. Pharm. Biomed. Anal. 2019, 172, 238–242. [Google Scholar] [CrossRef] [PubMed]
- Reddy, B.; Rozati, R.; Reddy, B.; Raman, N. Association of phthalate esters with endometriosis in India women. BJOG 2006, 113, 515–520. [Google Scholar] [CrossRef] [PubMed]
- Cobellis, L.; Latini, G.; De Felice, C.; Razzi, S.; Paris, I.; Ruggieri, F.; Mazzeo, P.; Petraglia, F. High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis. Hum. Reprod. 2003, 18, 1512–1515. [Google Scholar] [CrossRef]
- Huang, P.C.; Tsai, E.M.; Li, W.F.; Liao, P.C.; Chung, M.C.; Wang, Y.H.; Wang, S.L. Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum. Reprod. 2010, 25, 986–994. [Google Scholar] [CrossRef] [Green Version]
- Weuve, J.; Hauser, R.; Calafat, A.M.; Missmer, S.A.; Wise, L.A. Association of exposure to phthalates with endometriosis and uterine leiomyomata: Findings from NHANES, 1999–2004. Environ. Health Perspect. 2010, 118, 825–832. [Google Scholar] [CrossRef]
- Nazir, S.; Usman, Z.; Imran, M.; Lone, K.P.; Ahmad, G. Women Diagnosed with Endometriosis Show High Serum Levels of Diethyl Hexyl Phthalate. J. Hum. Reprod. Sci. 2018, 11, 131–136. [Google Scholar] [CrossRef]
- Louis Buck, G.M.; Peterson, C.M.; Chen, Z.; Croughan, M.; Sundaram, R.; Stanford, J.; Varner, M.W.; Kennedy, A.; Giudice, L.; Fujimoto, V.Y.; et al. Bisphenol A and phthalates and endometriosis: The Endometriosis: Natural History, Diagnosis and Outcomes Study. Fertil. Steril. 2013, 100, 162–169.e2. [Google Scholar] [CrossRef] [Green Version]
- Itoh, H.; Iwasaki, M.; Hanaoka, T.; Sasaki, H.; Tanaka, T.; Tsugane, S. Urinary phthalate monoesters and endometriosis in infertile Japanese women. Sci. Total Environ. 2009, 408, 37–42. [Google Scholar] [CrossRef]
- Kim, S.H.; Cho, S.; Ihm, H.J.; Oh, Y.S.; Heo, S.-H.; Chun, S.; Im, H.; Chae, H.D.; Kim, C.-H.; Moon, K.B. Possible Role of Phthalate in the Pathogenesis of Endometriosis: In Vitro, Animal, and Human Data. J. Clin. Endocrinol. Metab. 2015, 100, E1502–E1511. [Google Scholar] [CrossRef]
- Kim, S.H.; Chun, S.; Jang, J.Y.; Chae, H.D.; Kim, C.H.; Kang, B.M. Increased plasma levels of phthalate esters in women with advanced-stage endometriosis: A prospective case-control study. Fertil. Steril. 2011, 95, 357–359. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Lu, Y.; Ma, H.; Xu, Q.; Wu, X. Combined Exposure to Multiple Endocrine Disruptors and Uterine Leiomyomata and Endometriosis in US Women. Front. Endocrinol. 2021, 12, 726876. [Google Scholar] [CrossRef] [PubMed]
- Vandenberg, L.N.; Chahoud, I.; Heindel, J.J.; Padmanabhan, V.; Paumgartten, F.J.; Schoenfelder, G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ. Health Perspect. 2010, 118, 1055–1070. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Liao, C.; Liu, F.; Wu, Q.; Guo, Y.; Moon, H.B.; Nakata, H.; Kannan, K. Occurrence and human exposure of p-hydroxybenzoic acid esters (parabens), bisphenol A diglycidyl ether (BADGE), and their hydrolysis products in indoor dust from the United States and three East Asian countries. Environ. Sci. Technol. 2012, 21, 11584–11593. [Google Scholar] [CrossRef] [PubMed]
- Viñas, R.; Jeng, Y.J.; Watson, C.S. Non-genomic effects of xenoestrogen mixtures. Int. J. Environ. Res. Public Health 2012, 9, 2694–2714. [Google Scholar] [CrossRef] [PubMed]
- Rochester, J.R. Bisphenol A and human health: A review of the literature. Reprod. Toxicol. 2013, 42, 132–155. [Google Scholar] [CrossRef] [PubMed]
- Rubin, B.S. Bisphenol A: An endocrine disruptor with widespread exposure and multiple effects. J. Steroid. Biochem. Mol. Biol. 2011, 127, 27–34. [Google Scholar] [CrossRef]
- Vandenberg, L.N.; Colborn, T.; Hayes, T.B.; Heindel, J.J.; Jacobs, D.R., Jr.; Lee, D.-H.; Shioda, T.; Soto, A.M.; Saal, F.S.; Welshons, W.V.; et al. Hormones and Endocrine-Disrupting Chemicals: Low-Dose Effects and Nonmonotonic Dose Responses. Endocr. Rev. 2012, 33, 378–455. [Google Scholar] [CrossRef]
- Quesada, I.; Fuentes, E.; Viso-León, M.C.; Soria, B.; Ripoll, C.; Nadal, A. Low doses of the endocrine disruptor Bisphenol-A and the native hormone 17β-estradiol rapidly activate the transcription factor CREB. FASEB J. 2002, 16, 1671–1673. [Google Scholar] [CrossRef]
- Upson, K.; Sathyanarayana, S.; De Roos, A.J.; Koch, H.M.; Scholes, D.; Holt, V.L. A population-based case–control study of urinary bisphenol A concentrations and risk of endometriosis. Hum. Reprod. 2014, 29, 2457–2464. [Google Scholar] [CrossRef] [Green Version]
- Peinado, F.M.; Lendínez, I.; Sotelo, R.; Iribarne-Durán, L.M.; Fernández-Parra, J.; Vela-Soria, F.; Olea, N.; Fernández, M.F.; Freire, C.; León, J.; et al. Association of Urinary Levels of Bisphenols A, F, and S with Endometriosis Risk: Preliminary Results of the EndEA Study. Int. J. Environ. Res. Public Health 2020, 17, 1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rashidi, B.H.; Amanlou, M.; Lak, T.B.; Ghazizadeh, M.; Eslami, B. A case-control study of bisphenol A and endometrioma among subgroup of Iranian women. J. Res. Med. Sci. 2017, 22, 7. [Google Scholar] [CrossRef] [PubMed]
- Simonelli, A.; Guadagni, R.; De Franciscis, P.; Colacurci, N.; Pieri, M.; Basilicata, P.; Pedata, P.; Lamberti, M.; Sannolo, N.; Miraglia, N. Environmental and occupational exposure to bisphenol A and endometriosis: Urinary and peritoneal fluid concentration levels. Int. Arch. Occup. Environ. Health 2017, 90, 49–61. [Google Scholar] [CrossRef] [PubMed]
- Cobellis, L.; Colacurci, N.; Trabucco, E.; Carpentiero, C.; Grumetto, L. Measurement of bisphenol A and bisphenol B levels in human blood sera from healthy and endometriotic women. Biomed. Chromatogr. 2009, 23, 1186–1190. [Google Scholar] [CrossRef]
- Wen, X.; Xiong, Y.; Jin, L.; Zhang, M.; Huang, L.; Mao, Y.; Zhang, Y. Bisphenol A exposure enhances endometrial stromal cell invasion and has a positive association with peritoneal endometriosis. Reprod. Sci. 2020, 27, 704–712. [Google Scholar] [CrossRef]
- Itoh, H.; Iwasaki, M.; Hanaoka, T.; Sasaki, H.; Tanaka, T.; Tsugane, S. Urinary bisphenol-A concentration in infertile Japanese women and its association with endometriosis: A cross-sectional study. Environ. Health Prev. Med. 2007, 12, 258–264. [Google Scholar] [CrossRef]
- Nowak, K.; Ratajczak–Wrona, W.; Górska, M.; Jabłońska, E. Parabens and their effects on the endocrine system. Mol. Cell Endocrinol. 2018, 474, 238–251. [Google Scholar] [CrossRef]
- Boberg, J.; Taxvig, C.; Christiansen, S.; Hass, U. Possible endocrine disrupting effects of parabens and their metabolites. Reprod. Toxicol. 2010, 30, 301–312. [Google Scholar] [CrossRef]
- Darbre, P.D.; Harvey, P.W. Paraben esters: Review of recent studies of endocrine toxicity, absorption, esterase and human exposure, and discussion of potential human health risks. J. Appl. Toxicol. 2008, 28, 561–578. [Google Scholar] [CrossRef]
- Cho, Y.J.; Yun, J.H.; Kim, S.J.; Kwon, H.Y. Nonpersistent endocrine disrupting chemicals and reproductive health of women. Obstet. Gynecol. Sci. 2020, 63, 1–12. [Google Scholar] [CrossRef]
- Gao, C.-J.; Kannan, K. Phthalates, bisphenols, parabens, and triclocarban in feminine hygiene products from the United States and their implications for human exposure. Environ. Int. 2020, 136, 105465. [Google Scholar] [CrossRef] [PubMed]
- Peinado, F.M.; Ocón-Hernández, O.; Iribarne-Durán, L.M.; Vela-Soria, F.; Ubiña, A.; Padilla, C.; Mora, J.C.; Cardona, J.; León, J.; Fernández, M.F.; et al. Cosmetic and personal care product use, urinary levels of parabens and benzophenones, and risk of endometriosis: Results from the EndEA study. Environ. Res. 2021, 196, 110342. [Google Scholar] [CrossRef] [PubMed]
- Heurung, A.R.; Raju, S.I.; Warshaw, E.M. Benzophenones. Dermatitis 2014, 25, 3–10. [Google Scholar] [CrossRef] [PubMed]
- Long, J.; Xia, W.; Li, J.; Zhou, Y.; Zhao, H.; Wu, C.; Liao, J.; Jiang, Y.; Li, C.; Li, Y.; et al. Maternal urinary benzophenones and infant birth size: Identifying critical windows of exposure. Chemosphere. 2019, 219, 655–661. [Google Scholar] [CrossRef]
- Zheng, X.; Ren, X.-M.; Zhao, L.; Guo, L.-H. Binding and activation of estrogen related receptor γ as possible molecular initiating events of hydroxylated benzophenones endocrine disruption toxicity. Environ. Pollut. 2020, 263, 114656. [Google Scholar] [CrossRef]
- Kunisue, T.; Chen, Z.; Buck Louis, G.M.; Sundaram, R.; Hediger, M.L.; Sun, L.; Kannan, K. Urinary concentrations of benzophenone-type UV filters in US women and their association with endometriosis. Environ. Sci. Technol. 2012, 46, 4624–4632. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cecchi, A.; Rovedatti, M.G.; Sabino, G.; Magnarelli, G.G. Environmental exposure to organophosphate pesticides: Assessment of endocrine disruption and hepatotoxicity in pregnant women. Ecotoxicol. Environ. Saf. 2012, 80, 280–287. [Google Scholar] [CrossRef]
- Brander, S.M.; Gabler, M.K.; Fowler, N.L.; Connon, R.E.; Schlenk, D. Pyrethroid pesticides as endocrine disruptors: Molecular mechanisms in vertebrates with a focus on fishes. Environ. Sci. Technol. 2016, 50, 8977–8992. [Google Scholar] [CrossRef]
- Pope, C.N. Organophosphorus pesticides: Do they all have the same mechanism of toxicity? J. Toxicol. Environ. Health B 1999, 2, 161–181. [Google Scholar] [CrossRef]
- Jokanović, M.; Kosanović, M. Neurotoxic effects in patients poisoned with organophosphorus pesticides. Environ. Toxicol. Pharmacol. 2010, 29, 195–201. [Google Scholar] [CrossRef]
- Bell, E.M.; Hertz-Picciotto, I.; Beaumont, J.J. A Case-Control Study of Pesticides and Fetal Death Due to Congenital Anomalies. Epidemiology 2001, 12, 148–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yucra, S.; Rubio, J.; Gasco, M.; Gonzales, C.; Steenland, K.; Gonzales, G.F. Semen quality and reproductive sex hormone levels in Peruvian pesticide sprayers. Int. J. Occup. Environ. Health 2006, 12, 355–361. [Google Scholar] [CrossRef] [PubMed]
- Venkidasamy, B.; Subramanian, U.; Samynathan, R.; Rajakumar, G.; Shariati, M.A.; Chung, I.M.; Thiruvengadam, M. Organopesticides and fertility: Where does the link lead to? Environ. Sci. Pollut. Res. 2021, 28, 6289–6301. [Google Scholar] [CrossRef] [PubMed]
- Feo, M.L.; Eljarrat, E.; Barceló, D.; Barceló, D. Determination of pyrethroid insecticides in environmental samples. Trends Anal. Chem. 2010, 29, 692–705. [Google Scholar] [CrossRef]
- Ding, G.; Cui, C.; Chen, L.; Gao, Y.; Zhou, Y.; Shi, R.; Tian, Y. Prenatal exposure to pyrethroid insecticides and birth outcomes in Rural Northern China. J. Expo. Sci. Environ. Epidemiol. 2015, 25, 264–270. [Google Scholar] [CrossRef] [PubMed]
- Garey, J.; Wolff, M.S. Estrogenic and Antiprogestagenic Activities of Pyrethroid Insecticides. Biochem. Biophys. Res. Commun. 1998, 251, 855–859. [Google Scholar] [CrossRef] [PubMed]
- Li, A.J.; Chen, Z.; Lin, T.-C.; Louis, G.M.B.; Kannan, K. Association of urinary metabolites of organophosphate and pyrethroid insecticides, and phenoxy herbicides with endometriosis. Environ. Int. 2020, 136, 105456. [Google Scholar] [CrossRef]
- Meeker, J.D.; Barr, D.B.; Ryan, L.; Herrick, R.F.; Bennett, D.H.; Bravo, R.; Hauser, R. Temporal variability of urinary levels of nonpersistent insecticides in adult men. J. Expo. Anal. Environ. Epidemiol. 2005, 15, 271–281. [Google Scholar] [CrossRef]
Chemical Compound | Endometriosis |
---|---|
Phthalates: MEHP | + Upson et al. (2013) [41]; Fernandez et al. (2019) [42]; Louis et al. (2013) [48]; Kim et al. (2011) [51] - Cobellis et al. (2003) [44]; Huang et al. (2010) [45]; Weuve et al. (2010) [46]; Itoh et al. (2009) [49]; Zhang et al. (2021) [52] |
MEHHP | + Louis et al. (2013) [48]; Kim et al. (2015) [50] - Upson et al. (2013) [41]; Weuve et al. (2010) [46]; Itoh et al. (2009) [49]; Zhang et al. (2021) [52] |
MEOHP | + Louis et al. (2013) [48]; Kim et al. (2015) [50] - Upson et al. (2013) [41]; Weuve et al. (2010) [46]; Itoh et al. (2009) [49]; Zhang et al. (2021) [52] |
MECPP | + Louis et al. (2013) [48]; Kim et al. (2015) [50] - Upson et al. (2013) [41] |
MBzP | - Upson et al. (2013) [41]; Fernandez et al. (2019) [42]; Louis et al. (2013) [48]; Huang et al. (2010) [45]; Weuve et al. (2010) [46]; Itoh et al. (2009) [49]; Zhang et al. (2021) [52] |
MEP | - Upson et al. (2013) [41]; Huang et al. (2010) [45]; Weuve et al. (2010) [46]; Louis et al. (2013) [48]; Itoh et al. (2009) [49]; Zhang et al. (2021) [52] |
MiBP | - Upson et al. (2013) [41]; Fernandez et al. (2019) [42]; Louis et al. (2013) [48]; Zhang et al. (2021) [52] |
MnBP | + Huang et al. (2010) [45] - Upson et al. (2013) [41]; Itoh et al. (2009) [49]; Kim et al. (2015) [50] |
MMP | - Fernandez et al. (2019) [42]; Louis et al. (2013) [48]; Huang et al. (2010) [45] |
MBP | + Louis et al. (2013) [48] - Fernandez et al. (2019) [42]; Weuve et al. (2010) [46]; Zhang et al. (2021) [52] |
MCHP | - Fernandez et al. (2019) [42]; Louis et al. (2013) [48]; Zhang et al. (2021) [52] |
MiNP | - Fernandez et al. (2019) [42] |
DnBP | + Reddy et al. (2006) [43] |
BBP | + Reddy et al. (2006) [43] |
DnOP | + Reddy et al. (2006) [43] |
DEHP | + Reddy et al. (2006) [43]; Nair et al. (2018) [47] - Cobellis et al. (2003) [44]; Kim et al. (2011) [51] |
5oxo-MEHP | - Huang et al. (2010) [45] |
5OH-MEHP | - Huang et al. (2010) [45] |
MCPP | - Louis et al. (2013) [48]; Zhang et al. (2021) [52] |
MCMHP | + Louis et al. (2013) [48] |
MNP | - Zhang et al. (2021) [52] |
MOP | - Fernandez et al. (2019) [42]; Zhang et al. (2021) [52] |
MNM | - Zhang et al. (2021) [52] |
Bisphenol A | + Upson (2014) [60]; Peinado et al. (2020) [61]; Rashidi et al. (2017) [62]; Simonelli et al. (2016) [63]; Wen et al. (2020) [65] - Fernandez et al. (2019) [42]; Louis et al. (2013) [48]; Cobellis et al. (2009) [64]; Itoh et al. (2007) [66] |
Parabens: MeP | + Peinado et al. (2020) [72] |
EtP | - Peinado et al. (2020) [72] |
PrP | - Peinado et al. (2020) [72] |
BuP | - Peinado et al. (2020) [72] |
Benophenones: BP-1 | + Peinado et al. (2020) [72] |
BP-3 | + Peinado et al. (2020) [72] |
4-OH-BP | - Peinado et al. (2020) [72]; Kunisue et al. (2012) [76] |
2OH-4MeO-BP | - Kunisue et al. (2012) [76] |
2,4OH-BP | - Kunisue et al. (2012) [76] |
Non persistent pesticides: IMPY | + Li et al. (2020) [87] |
MDA | - Li et al. (2020) [87] |
PNP | - Li et al. (2020) [87] |
TCPY | + Li et al. (2020) [87] |
2,4-D | - Li et al. (2020) [87] |
2,4,5-T | - Li et al. (2020) [87] |
3-PBA | - Li et al. (2020) [87] |
4F-3PBA | - Li et al. (2020) [87] |
trans-DCCA | - Li et al. (2020) [87] |
cis-DCCA | - Li et al. (2020) [87] |
cis-DBCA | - Li et al. (2020) [87] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wieczorek, K.; Szczęsna, D.; Jurewicz, J. Environmental Exposure to Non-Persistent Endocrine Disrupting Chemicals and Endometriosis: A Systematic Review. Int. J. Environ. Res. Public Health 2022, 19, 5608. https://doi.org/10.3390/ijerph19095608
Wieczorek K, Szczęsna D, Jurewicz J. Environmental Exposure to Non-Persistent Endocrine Disrupting Chemicals and Endometriosis: A Systematic Review. International Journal of Environmental Research and Public Health. 2022; 19(9):5608. https://doi.org/10.3390/ijerph19095608
Chicago/Turabian StyleWieczorek, Katarzyna, Dorota Szczęsna, and Joanna Jurewicz. 2022. "Environmental Exposure to Non-Persistent Endocrine Disrupting Chemicals and Endometriosis: A Systematic Review" International Journal of Environmental Research and Public Health 19, no. 9: 5608. https://doi.org/10.3390/ijerph19095608