Exposure to Endocrine Disrupting Chemicals and Risk of Breast Cancer
Abstract
:1. Introduction
2. Breast Cancer, the Most Common Cancer in Women Sill on the Rise
2.1. Specificities of the Mammary Gland and Its Windows of Susceptibility
2.2. Complementary Classifications of Breast Cancer
2.3. A Complex Combination of Risk Factors
3. Difficult Identification of the Mode of Action of Endocrine Disrupting Chemicals
3.1. A Recent Concept in Constant Evolution
3.2. Effects of Endocrine Disrupting Chemicals on Hormone Signaling
3.2.1. Agonistic or Antagonistic Action on Different Hormone Receptors
3.2.2. Modification of the Level of Bioavailable Endogenous Hormones
3.2.3. Alteration of the Cell Epigenome
4. Case Studies of Endocrine Disrupting Chemicals Linked with Increased Risk of Breast Cancer
4.1. Endocrine Disrupting Chemicals and Medicine: Diethylstilbestrol in Pregnant Women
4.1.1. Diethylstilbestrol, a Synthetic Estrogen Inducing Significant Epigenetic Changes
4.1.2. Diethylstilbestrol during Pregnancy: Three Generations Impacted
4.1.3. Indication and Use of Diethylstilbestrol after the Tragedy
4.2. Massive Use of Dichlorodiphenyltrichloroethane: Awareness of Environmental Pollution by Toxic Endocrine Disruptor Chemicals
4.2.1. The Dual Mode of Action of Dichlorodiphenyltrichloroethane, Both Estrogenic Agonist and Androgenic Antagonist
4.2.2. Prepubertal Exposure to Dichlorodiphenyltrichloroethane and Breast Cancer Occurrence
4.2.3. Partial Ban of Dichlorodiphenyltrichloroethane and Current Regulations
4.3. Industrial Accident and Release of Toxic Dioxins into the Environment: Current Exposure and Risks
4.3.1. 2,3,7,8-tetrachlorodibenzo-p-dioxin, a Potent Agonist of the Aryl Hydrocarbon Receptor
4.3.2. Exposure to Toxic Dioxins and Breast Cancer Risk: Heterogeneous Results
4.3.3. Industrial Risk Management and Control of Dioxin Release
4.4. Bisphenol A: Difficulty in Tracing Exposure to a Synthetic Estrogen Ubiquitously Present in the Environment
4.4.1. Bisphenol A, a Synthetic Estrogen Similar to Diethylstilbestrol
4.4.2. A Ubiquitous Presence Making Epidemiological Studies Difficult
4.4.3. The Precautionary Principle behind Bisphenol A Legislation in Some Countries
5. Discussion
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
ADI | Acceptable Daily Intake |
AhR | Aryl hydrocarbon Receptor |
AR | Androgen Receptor |
BC | Breast Cancer |
BMI | Body Mass Index |
BPA | Bisphenol A |
BRCA1/2 | Breast Cancer type 1/2 susceptibility protein |
DDE | Dichlorodiphenyldichloroethylene |
DDT | Dichlorodiphenyltrichloroethane |
DES | Diethylstilbestrol or stilbestrol |
DNMTs | DNA methyltransferases |
EDCs | Endocrine Disrupting Chemicals |
EPA | Environmental Protection Agency |
ERα/β | Estrogen Receptor α/β |
ERE | Estrogen Response Elements |
ERRγ | Estrogen-Related Receptor γ |
FDA | Food and Drug Administration |
GPR30 | G Protein-coupled Receptor 30 |
HER2 | Human Epidermal Growth Factor Receptor 2 |
HRT | Hormone Replacement Therapy |
IARC | International Agency for Research on Cancer |
LOAEL | Lowest Observed Adverse Effect Level |
miRNA | microRNA |
mRNA | messenger RNA |
NOAEL | No Observable Adverse Effect Level |
PDCD4 | Programmed Cell Death Protein 4 |
POP | Persistent Organic Pollutant |
PR | Progesterone Receptor |
SR | Steroid Receptor |
TCDD | 2,3,7,8-tetrachlorodibenzo-p-dioxin |
TEB | Terminal End Buds |
TEQ | Toxic Equivalent |
TNBC | Triple Negative Breast Cancer |
WHO | World Health Organization |
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Risk | Example | Impact | Refs |
---|---|---|---|
Reproductive factors | Age at menarche | BC risk decreases by 5% for each year without menstruation between 11 and 17 years of age | [29] |
Age at menopause | BC risk decreases by 3% for each year without being menopausal between 35 and 55 years of age | ||
Age at first birth | BC risk increases by 3% before menopause and 5% after menopause for each year that first full-term pregnancy is delayed | [30] | |
Parity | Each full-term pregnancy decreases BC risk by 3% before menopause and 12% after menopause | ||
Breastfeeding | Breastfeeding decreases BC risk by 14% before menopause and 11% after menopause | [31] | |
Exogenous hormones | Combined hormonal replacement therapy (HRT) | BC risk increases by 60% for 1 to 4 years of use and by 108% for more than 5 years of combined HRT use | [10] |
Hormonal contraception | BC risk increases by 0.7% for each year of contraceptive use | [11] | |
Anthropometric factors | Body mass index (BMI) | The risk of postmenopausal BC increases by 40% for every 10-point increase in BMI | [32] |
Sex and age | Sex | Less than 1% of BC develop in men | [33] |
Age | More than 70% of BC are diagnosed after 50 years of age | [2] | |
Breast density and personal history of BC | Breast density | A 5% increase in breast density increases BC risk by 5 to 10% | [34] |
Personal history | Surviving BC increases the risk of developing second primary BC by 74% | [35] | |
Familial history of BC | First-degree family history | One history of BC increases the risk by 77% Two or more histories of BC increase the risk by 250% | [36] |
Breast cancer type 1 susceptibility protein mutation | 55% risk of developing BC after 70 years of age | [37] | |
Breast cancer type 2 susceptibility protein mutation | 47% risk of developing BC after 70 years of age | ||
Lifestyle | Diet | Consumption of 120 g per day of red meat increases BC risk by 11% | [38] |
Tobacco | BC risk increases by 0.5% for each year of smoking | [39] | |
Alcohol | Every unit of alcohol (10 g of alcohol) drunk per day increases BC risk by 7% | [40] | |
Physical activity | BC risk decreases by 18% with the practice of 1 to 3 h of physical activity per week and 21% for more than 7 h per week | [41] | |
Occupation | Night shift work | 20 years or more of rotating nightshift work at baseline induce a 2-fold increase in BC risk 20 years or more of cumulative rotating night-shift work increases BC risk by 40% | [42] |
Exposure to radiation | Hodgkin lymphoma radiation | 29% risk of developing BC after 55 years of age for women who received chest radiation before 25 years of age | [43] |
Author (Year) | Study Years | Country | Design | Cases/Controls | Exposure Assessment | Results |
---|---|---|---|---|---|---|
Bibbo (1978) [108] | 1976–1977 | USA | Prospective | 693/668 | Participants in the 1951 clinical study | No significant increase in BC risk in DES mothers |
Greenberg (1984) [109] | 1981 | USA | Prospective | 2885/2816 | Obstetric records | Significant increase in BC risk for DES mothers exposed more than 30 years prior the study (RR = 2.5; 95% CI: 1.1–5.8) |
Colton (1993) [110] | 1986–1989 | USA | Prospective | 2590/2471 | Obstetric records | Significant increase in BC risk for DES mothers after 60 years of age (RR = 1.47; 95% CI: 1.02–2.13) |
Titus-Ernstoff (2001) [111] | 1992–1994 | USA | Prospective | 2434/2402 | Obstetric records | Significant increase in BC risk for DES mothers exposed less than 40 years prior the study (RR = 1.27; 95% CI: 1.07–1.52) |
Hatch (1998) [112] | 1978–1994 | USA | Prospective | 3650/1202 | Obstetric records | No significant increase in BC risk in DES daughters (RR = 1.18; 95% CI: 0.56–2.49) |
Palmer (2006) [113] | 1978–2003 | USA | Prospective | 3812/1637 | Obstetric records | DES daughters have a significantly increased BC risk after 40 years of age (RR = 1.91; 95% CI: 1.09–3.33) and after 50 years of age (RR = 3.00; 95% CI: 1.01–8.98) |
Troisi (2007) [62] | 1978–2001 | USA | Prospective | 3813/1642 | Obstetric records | DES daughters have a significantly increased BC risk after 40 years of age (RR = 1.83; 95% CI: 1.1–3.2) |
Hoover (2011) [114] | 1975–2001 | USA | Prospective | 3796/1659 | Obstetric records | DES daughters have a significantly increased BC risk after 40 years of age (HR = 1.82; 95% CI: 1.04–3.18) |
Troisi (2019) [115] | 1994–2011 | USA | Prospective | 4822/2083 | Obstetric records | DES daughters have a significantly increased BC risk between 40 and 49 years of age (RR = 1.33; 95% CI: 1.05–1.66) |
Tournaire (2015) [116] | 2013 | France | Prospective | 3436/3256 | Self-report or medical records | DES daughters have a significantly increased BC risk (RR = 2.10; 95% CI: 1.60–2.76) but risk varies with low (RR = 1.63; 95% CI: 0.87–3.08) or high (RR = 2.16; 95% CI: 1.18–3.96) DES dose |
Verloop (2010) [117] | 1992–2008 | Netherlands | Prospective | 12,091 participants | Self-report or medical records | No significantly increase in BC risk in DES daughters (RR = 1.05; 95% CI: 0.90–1.23) |
Titus (2019) [118] | 2001–2012 | USA | Prospective | 796/469 | Obstetric records | DES granddaughters have genital malformations and other health problems similar to those of DES daughters |
Author (Year) | Study Years | Country | Design | Cases/Controls | Exposure Assessment | Results |
---|---|---|---|---|---|---|
Cohn (2007) [143] | 2000–2001 | USA | Prospective | 129/129 | Serum (1959–1967) | High DDT serum concentrations are associated with a significant increase in BC risk in women born after 1931 (OR = 5.4; 95% CI: 1.7–17.1) |
Cohn (2015) [144] | 2010–2013 | USA | Prospective | 103/315 | Serum (1959–1967) | High DDT serum concentrations in mothers are associated with a significant increase in BC risk (OR = 3.7; 95% CI: 1.5–9.0); advanced stage at diagnosis (OR = 4.6; 95% CI: 1.3–16.5); and Human Epidermal Growth Factor Receptor 2 + (HER2+) tumors in daughters (OR = 2.1; 95% CI: 1.0–4.8) |
Cohn (2019) [145] | 1970–2010 | USA | Prospective | 146/422 | Serum (1959–1967) | Exposure to DDT after 4 years of age significantly increases the risk of BC diagnosed before the age of 54 (OR = 3.70; 95% CI: 1.22–11.26) |
White (2013) [146] | NA | USA | Retrospective | 1508/1556 | Residential exposure by questionnaire | Women with hormone-dependent BC have a significantly greater risk of having ever seen spreaders (OR = 1.44; 95% CI: 1.08–1.93) Women with Estrogen Receptor + (ER+) or Progesterone Receptor + (PR+) BC have a significantly increased odds of ever seeing a fogger truck (OR = 1.33; 95% CI: 1.11–1.59) |
Niehoff (2016) [147] | 2003–2009 | USA + Puerto Rico | Prospective | 2134 participants | Residential exposure by questionnaire | No significant association between having ever seen a spreader before DDT ban and BC risk (HR = 1.3; 95% CI: 0.92–1.7) |
Bachelet (2019) [148] | NA | France | Retrospective | 695/1055 | Serum (2005–2007) | No significant association between high DDE serum concentrations and BC risk (OR = 0.93; 95% CI: 0.73–1.18) |
Itoh (2009) [149] | NA | Japan | Retrospective | 403/403 | Serum (2001–2005) | No significant association between high DDT serum concentrations and BC risk (OR = 0.58; 95% CI: 0.27–1.25) |
Ingber (2013) [150] | 2012 | Multi-centric | Meta-analysis | 40 DDT or DDE studies | Serum | No significant association between BC risk and high serum concentrations of DDT (OR = 1.02; 95% CI: 0.92–1.13) or DDE (OR = 1.04; 95% CI: 0.94–1.15) |
Park (2014) [142] | 2012 | Multi-centric | Meta-analysis | 35 DDE studies | Serum | No significant association between high DDE serum concentrations and BC risk (OR = 1.03; 95% CI: 0.95–1.12) |
Author (Year) | Study Years | Country | Design | Cases/Controls | Exposure Assessment | Results |
---|---|---|---|---|---|---|
Warner (2002) [190] | 1996–1998 | Italy | Prospective | 981 participants | Serum (1976–1981) | A 10-fold increase in TCDD plasma concentrations was associated with an increase in BC risk (HR = 2.1; 95% CI: 1.0–4.6) |
Warner (2011) [191] | 1996–2008 | Italy | Prospective | 833 participants | Serum (1976–1981) | No association between high TCDD serum concentrations and BC risk (HR = 1.44; 95% CI: 0.89–2.33) |
Pesatori (2009) [192] | 2006-2009- | Italy | Prospective | 2122 participants | Medical records (1992–1996) | Living near the chemical plant during the accident significantly increases BC risk (RR = 2.57; 95% CI: 1.07–6.20) |
Revich (2001) [189] | 1997–1998 | Russia | Prospective | 14 participants | Human milk and serum (1997–1998) | BC incidence and mortality are doubled in Chapayevsk compared to the national average |
Danjou (2015) [193] | 1993–2008 | France | Prospective | 63,830 participants | Dietary exposure | No significant association between higher dietary dioxin exposure and BC risk (HR = 1.00; 95% CI: 0.96–1.05) |
Danjou (2019) [194] | 1993–2008 | France | Prospective | 429/716 | Airborne exposure | No significant association between higher estimated airborne dioxin exposure and BC risk (OR = 1.124; 95% CI: 0.693–1.824) |
VoPham (2020) [195] | 1989–2013 | USA | Prospective | 112,397 participants | Airborne exposure | Living less than 10 km from a municipal solid waste incinerator significantly increases BC risk (HR = 1.15; 95% CI: 1.03–1.28) The risk increases again by living less than 5 km away (HR = 1.25; 95% CI: 1.04–1.52) |
Xu (206) [196] | 2015 | Multi-centric | Meta-analysis | 3 studies | Various | No significant association between higher TCDD exposure and BC risk (RR = 0.99; 95% CI: 0.93–1.06) |
Author (Year) | Study Years | Country | Design | Cases/Controls | Exposure Assessment | Results |
---|---|---|---|---|---|---|
Lang (2008) [237] | 2003–2004 | USA | Retrospective | 1455 participants | Urine (2003–2004) | No significant association between high urinary BPA levels and cancer risk (including BC) (OR = 1.12; 95% CI: 0.85–1.48) |
Trabert (2014) [238] | 2000–2003 | Poland | Retrospective | 575/575 | Urine (2000–2003) | No significant association between high urinary BPA levels and postmenopausal BC risk (OR = 1.09; 95% CI: 0.73–1.63) |
Yang (2009) [239] | 2004–2007 | Korea | Prospective | 70/82 | Serum (1994–1997) | Significant association between high serum BPA levels and nulliparity (p < 0.05) No significant association between BPA levels and BC risk (p = 0.42) |
Sprague (2013) [240] | 2008–2009 | USA | Retrospective | 264 participants | Serum (2008–2009) | Significant association between high serum BPA levels and high breast density (p = 0.01) |
Binder (2018) [241] | 2006 | Chile | Prospective | 200 participants | Urine (2006) | Significant association between lower and higher urine BPA levels and high breast density (p < 0.01) |
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Eve, L.; Fervers, B.; Le Romancer, M.; Etienne-Selloum, N. Exposure to Endocrine Disrupting Chemicals and Risk of Breast Cancer. Int. J. Mol. Sci. 2020, 21, 9139. https://doi.org/10.3390/ijms21239139
Eve L, Fervers B, Le Romancer M, Etienne-Selloum N. Exposure to Endocrine Disrupting Chemicals and Risk of Breast Cancer. International Journal of Molecular Sciences. 2020; 21(23):9139. https://doi.org/10.3390/ijms21239139
Chicago/Turabian StyleEve, Louisane, Béatrice Fervers, Muriel Le Romancer, and Nelly Etienne-Selloum. 2020. "Exposure to Endocrine Disrupting Chemicals and Risk of Breast Cancer" International Journal of Molecular Sciences 21, no. 23: 9139. https://doi.org/10.3390/ijms21239139