Serum Levels of Commonly Detected Persistent Organic Pollutants and Per- and Polyfluoroalkyl Substances (PFASs) and Mammographic Density in Postmenopausal Women
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Centers for Disease Control and Prevention. Fourth Report on Human Exposure to Environmental Chemicals. Available online: https://www.cdc.gov/exposurereport (accessed on 1 October 2019).
- Lauby-Secretan, B.; Loomis, D.; Baan, R.; El Ghissassi, F.; Bouvard, V.; Benbrahim-Tallaa, L.; Guha, N.; Grosse, Y.; Straif, K. Use of mechanistic data in the IARC evaluations of the carcinogenicity of polychlorinated biphenyls and related compounds. Environ. Sci. Pollut. Res. Int. 2016, 23, 2220–2229. [Google Scholar] [CrossRef] [PubMed]
- Xue, J.; Liu, S.V.; Zartarian, V.G.; Geller, A.M.; Schultz, B.D. Analysis of NHANES measured blood PCBs in the general US population and application of SHEDS model to identify key exposure factors. J. Expo. Sci. Environ. Epidemiol. 2014, 24, 615–621. [Google Scholar] [CrossRef] [PubMed]
- Petreas, M.; Smith, D.; Hurley, S.; Jeffrey, S.S.; Gilliss, D.; Reynolds, P. Distribution of persistent, lipid-soluble chemicals in breast and abdominal adipose tissues: Lessons learned from a breast cancer study. Cancer Epidemiol. Biomark. Prev. 2004, 13, 416–424. [Google Scholar]
- Leng, L.; Li, J.; Luo, X.M.; Kim, J.Y.; Li, Y.M.; Guo, X.M.; Chen, X.; Yang, Q.Y.; Li, G.; Tang, N.J. Polychlorinated biphenyls and breast cancer: A congener-specific meta-analysis. Environ. Int. 2016, 88, 133–141. [Google Scholar] [CrossRef]
- IARC. Polychlorinated biphenyls and polybrominated biphenyls. In IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; IARC: Lyon, France, 2015; Volume 107. [Google Scholar]
- Negri, E.; Bosetti, C.; Fattore, E.; La Vecchia, C. Environmental exposure to polychlorinated biphenyls (PCBs) and breast cancer: A systematic review of the epidemiological evidence. Eur. J. Cancer Prev. 2003, 12, 509–516. [Google Scholar] [CrossRef]
- Gatto, N.M.; Longnecker, M.P.; Press, M.F.; Sullivan-Halley, J.; McKean-Cowdin, R.; Bernstein, L. Serum organochlorines and breast cancer: A case-control study among African-American women. Cancer Causes Control. 2007, 18, 29–39. [Google Scholar] [CrossRef] [Green Version]
- Itoh, H.; Iwasaki, M.; Hanaoka, T.; Kasuga, Y.; Yokoyama, S.; Onuma, H.; Nishimura, H.; Kusama, R.; Tsugane, S. Serum organochlorines and breast cancer risk in Japanese women: A case-control study. Cancer Causes Control. 2009, 20, 567–580. [Google Scholar] [CrossRef]
- Laden, F.; Collman, G.; Iwamoto, K.; Alberg, A.J.; Berkowitz, G.S.; Freudenheim, J.L.; Hankinson, S.E.; Helzlsouer, K.J.; Holford, T.R.; Huang, H.Y.; et al. 1,1-Dichloro-2,2-bis(p-chlorophenyl)ethylene and polychlorinated biphenyls and breast cancer: Combined analysis of five U.S. studies. J. Natl. Cancer Inst. 2001, 93, 768–776. [Google Scholar] [CrossRef] [Green Version]
- Laden, F.; Ishibe, N.; Hankinson, S.E.; Wolff, M.S.; Gertig, D.M.; Hunter, D.J.; Kelsey, K.T. Polychlorinated biphenyls, cytochrome P450 1A1, and breast cancer risk in the Nurses’ Health Study. Cancer Epidemiol. Biomark. Prev. 2002, 11, 1560–1565. [Google Scholar]
- He, Y.; Peng, L.; Zhang, W.; Liu, C.; Yang, Q.; Zheng, S.; Bao, M.; Huang, Y.; Wu, K. Adipose tissue levels of polybrominated diphenyl ethers and breast cancer risk in Chinese women: A case-control study. Environ. Res. 2018, 167, 160–168. [Google Scholar] [CrossRef]
- Hurley, S.; Goldberg, D.; Wang, M.; Park, J.S.; Petreas, M.; Bernstein, L.; Anton-Culver, H.; Nelson, D.O.; Reynolds, P. Breast cancer risk and serum levels of per- and poly-fluoroalkyl substances: A case-control study nested in the California Teachers Study. Environ. Health 2018, 17, 83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hurley, S.; Goldberg, D.; Park, J.S.; Petreas, M.; Bernstein, L.; Anton-Culver, H.; Neuhausen, S.L.; Nelson, D.O.; Reynolds, P. A breast cancer case-control study of polybrominated diphenyl ether (PBDE) serum levels among California women. Environ. Int. 2019, 127, 412–419. [Google Scholar] [CrossRef] [PubMed]
- Holmes, A.K.; Koller, K.R.; Kieszak, S.M.; Sjodin, A.; Calafat, A.M.; Sacco, F.D.; Varner, D.W.; Lanier, A.P.; Rubin, C.H. Case-control study of breast cancer and exposure to synthetic environmental chemicals among Alaska Native women. Int. J. Circumpolar Health 2014, 73, 25760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hurley, S.; Reynolds, P.; Goldberg, D.; Nelson, D.O.; Jeffrey, S.S.; Petreas, M. Adipose levels of polybrominated diphenyl ethers and risk of breast cancer. Breast Cancer Res. Treat. 2011, 129, 505–511. [Google Scholar] [CrossRef]
- Bonefeld-Jorgensen, E.C.; Long, M.; Fredslund, S.O.; Bossi, R.; Olsen, J. Breast cancer risk after exposure to perfluorinated compounds in Danish women: A case-control study nested in the Danish National Birth Cohort. Cancer Causes Control. 2014, 25, 1439–1448. [Google Scholar] [CrossRef] [Green Version]
- Barry, V.; Winquist, A.; Steenland, K. Perfluorooctanoic acid (PFOA) exposures and incident cancers among adults living near a chemical plant. Environ. Health Perspect. 2013, 121, 1313–1318. [Google Scholar] [CrossRef] [Green Version]
- Vieira, V.M.; Hoffman, K.; Shin, H.M.; Weinberg, J.M.; Webster, T.F.; Fletcher, T. Perfluorooctanoic acid exposure and cancer outcomes in a contaminated community: A geographic analysis. Environ. Health Perspect. 2013, 121, 318–323. [Google Scholar] [CrossRef] [Green Version]
- Wielsoe, M.; Kern, P.; Bonefeld-Jorgensen, E.C. Serum levels of environmental pollutants is a risk factor for breast cancer in Inuit: A case control study. Environ. Health 2017, 16, 56. [Google Scholar] [CrossRef] [Green Version]
- Mancini, F.R.; Cano-Sancho, G.; Gambaretti, J.; Marchand, P.; Boutron-Ruault, M.C.; Severi, G.; Arveux, P.; Antignac, J.P.; Kvaskoff, M. Perfluorinated alkylated substances serum concentration and breast cancer risk: Evidence from a nested case-control study in the French E3N cohort. Int. J. Cancer 2019. [Google Scholar] [CrossRef]
- Kachuri, L.; Villeneuve, P.; Siddique, S.; Kubwabo, C.; Latifovic, L.; Boucher, B.; Ritter, L.; Cotterchio, M.; Knight, J.; Harris, S. Serum concentrations of Polybrominated Diphenyl Ethers (PBDEs) and breast cancer risk in young women: Results from the Ontario Environment and Health Study. Environ. Health Perspect. 2018, 2018, 1. [Google Scholar] [CrossRef]
- Boyd, N.F.; Guo, H.; Martin, L.J.; Sun, L.; Stone, J.; Fishell, E.; Jong, R.A.; Hislop, G.; Chiarelli, A.; Minkin, S.; et al. Mammographic density and the risk and detection of breast cancer. N. Engl. J. Med. 2007, 356, 227–236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolfe, J.N. Risk for breast cancer development determined by mammographic parenchymal pattern. Cancer 1976, 37, 2486–2492. [Google Scholar] [CrossRef]
- McCormack, V.A.; dos Santos Silva, I. Breast density and parenchymal patterns as markers of breast cancer risk: A meta-analysis. Cancer Epidemiol. Biomark. Prev. 2006, 15, 1159–1169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boyd, N.F.; Martin, L.J.; Rommens, J.M.; Paterson, A.D.; Minkin, S.; Yaffe, M.J.; Stone, J.; Hopper, J.L. Mammographic density: A heritable risk factor for breast cancer. Methods Mol. Biol. 2009, 472, 343–360. [Google Scholar] [CrossRef] [PubMed]
- Vachon, C.M.; Kuni, C.C.; Anderson, K.; Anderson, V.E.; Sellers, T.A. Association of mammographically defined percent breast density with epidemiologic risk factors for breast cancer (United States). Cancer Causes Control. 2000, 11, 653–662. [Google Scholar] [CrossRef] [PubMed]
- Woolcott, C.G.; Koga, K.; Conroy, S.M.; Byrne, C.; Nagata, C.; Ursin, G.; Vachon, C.M.; Yaffe, M.J.; Pagano, I.; Maskarinec, G. Mammographic density, parity and age at first birth, and risk of breast cancer: An analysis of four case-control studies. Breast Cancer Res. Treat. 2012, 132, 1163–1171. [Google Scholar] [CrossRef] [Green Version]
- Greendale, G.A.; Reboussin, B.A.; Sie, A.; Singh, H.R.; Olson, L.K.; Gatewood, O.; Bassett, L.W.; Wasilauskas, C.; Bush, T.; Barrett-Connor, E. Effects of estrogen and estrogen-progestin on mammographic parenchymal density. Postmenopausal Estrogen/Progestin Interventions (PEPI) Investigators. Ann. Intern. Med. 1999, 130, 262–269. [Google Scholar] [CrossRef]
- Greendale, G.A.; Reboussin, B.A.; Slone, S.; Wasilauskas, C.; Pike, M.C.; Ursin, G. Postmenopausal hormone therapy and change in mammographic density. J. Natl. Cancer Inst. 2003, 95, 30–37. [Google Scholar] [CrossRef] [Green Version]
- Terry, M.B.; Michels, K.B.; Brody, J.G.; Byrne, C.; Chen, S.; Jerry, D.J.; Malecki, K.M.C.; Martin, M.B.; Miller, R.L.; Neuhausen, S.L.; et al. Environmental exposures during windows of susceptibility for breast cancer: A framework for prevention research. Breast Cancer Res. 2019, 21, 96. [Google Scholar] [CrossRef] [Green Version]
- Binder, A.M.; Corvalan, C.; Pereira, A.; Calafat, A.M.; Ye, X.; Shepherd, J.; Michels, K.B. Prepubertal and Pubertal Endocrine-Disrupting Chemical Exposure and Breast Density among Chilean Adolescents. Cancer Epidemiol. Biomark. Prev. 2018, 27, 1491–1499. [Google Scholar] [CrossRef] [Green Version]
- Adams, S.V.; Newcomb, P.A.; Shafer, M.M.; Atkinson, C.; Bowles, E.J.; Newton, K.M.; Lampe, J.W. Urinary cadmium and mammographic density in premenopausal women. Breast Cancer Res. Treat. 2011, 128, 837–844. [Google Scholar] [CrossRef] [Green Version]
- Peplonska, B.; Bukowska, A.; Sobala, W.; Reszka, E.; Gromadzinska, J.; Wasowicz, W.; Lie, J.A.; Kjuus, H.; Ursin, G. Rotating night shift work and mammographic density. Cancer Epidemiol. Biomark. Prev. 2012, 21, 1028–1037. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stone, J.; Willenberg, L.; Apicella, C.; Treloar, S.; Hopper, J. The association between mammographic density measures and aspirin or other NSAID use. Breast Cancer Res. Treat. 2012, 132, 259–266. [Google Scholar] [CrossRef] [PubMed]
- Hiatt, R.A.; Haslam, S.Z.; Osuch, J. The breast cancer and the environment research centers: Transdisciplinary research on the role of the environment in breast cancer etiology. Environmental Health Perspect. 2009, 117, 1814–1822. [Google Scholar] [CrossRef] [PubMed]
- Bernstein, L.; Allen, M.; Anton-Culver, H.; Deapen, D.; Horn-Ross, P.L.; Peel, D.; Pinder, R.; Reynolds, P.; Sullivan-Halley, J.; West, D.; et al. High breast cancer incidence rates among California teachers: Results from the California Teachers Study (United States). Cancer Causes Control 2002, 13, 625–635. [Google Scholar] [CrossRef] [PubMed]
- Lee, E.; Ingles, S.A.; Van Den Berg, D.; Wang, W.; Lavallee, C.; Huang, M.H.; Crandall, C.J.; Stanczyk, F.Z.; Greendale, G.A.; Ursin, G. Progestogen levels, progesterone receptor gene polymorphisms, and mammographic density changes: Results from the Postmenopausal Estrogen/Progestin Interventions Mammographic Density Study. Menopause 2012, 19, 302–310. [Google Scholar] [CrossRef] [Green Version]
- Ursin, G.; Astrahan, M.A.; Salane, M.; Parisky, Y.R.; Pearce, J.G.; Daniels, J.R.; Pike, M.C.; Spicer, D.V. The detection of changes in mammographic densities. Cancer Epidemiol. Biomark. Prev. 1998, 7, 43–47. [Google Scholar]
- Morello-Frosch, R.; Cushing, L.J.; Jesdale, B.M.; Schwartz, J.M.; Guo, W.; Guo, T.; Wang, M.; Harwani, S.; Petropoulou, S.E.; Duong, W.; et al. Environmental Chemicals in an Urban Population of Pregnant Women and Their Newborns from San Francisco. Environ. Sci. Technol. 2016, 50, 12464–12472. [Google Scholar] [CrossRef]
- Diorio, C.; Dumas, I.; Sandanger, T.M.; Ayotte, P. Levels of circulating polychlorinated biphenyls and mammographic breast density. Anticancer Res. 2013, 33, 5483–5489. [Google Scholar]
- Wielsoe, M.; Eiberg, H.; Ghisari, M.; Kern, P.; Lind, O.; Bonefeld-Jorgensen, E.C. Genetic Variations, Exposure to Persistent Organic Pollutants and Breast Cancer Risk - A Greenlandic Case-Control Study. Basic Clin. Pharmacol. Toxicol. 2018, 123, 335–346. [Google Scholar] [CrossRef] [Green Version]
- Ghisari, M.; Long, M.; Roge, D.M.; Olsen, J.; Bonefeld-Jorgensen, E.C. Polymorphism in xenobiotic and estrogen metabolizing genes, exposure to perfluorinated compounds and subsequent breast cancer risk: A nested case-control study in the Danish National Birth Cohort. Environ. Res. 2017, 154, 325–333. [Google Scholar] [CrossRef] [PubMed]
- Database of Single Nucleotide Polymorphisms (dbSNP). Bethesda (MD): National Center for Biotechnology Information, National Library of Medicine. Available online: http://www.ncbi.nlm.nih.gov/SNP/ (accessed on 1 July 2017).
- Rattan, S.; Zhou, C.; Chiang, C.; Mahalingam, S.; Brehm, E.; Flaws, J.A. Exposure to endocrine disruptors during adulthood: Consequences for female fertility. J. Endocrinol. 2017, 233, R109–R129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Characteristics | Mean ± SD | N (%) |
---|---|---|
Age at Mammogram (Years) | 69.2 ± 4.9 | |
Age at Blood Draw (Years) | 67.9 ± 4.9 | |
Body Mass Index (BMI) at Mammogram (kg/m2) | 25.3 ± 4.8 | |
Mammographic Density (Percent) | 14.1 ± 13.1 | |
Estrogen–progestin Combined Hormone Therapy at Mammogram | ||
Never | 74 (64%) | |
Former Use | 34 (29%) | |
Current Use | 8 (7%) | |
Total Number of Births | ||
0 | 37 (32%) | |
1−2 | 58 (50%) | |
3+ | 21 (18%) | |
Time Interval between Mammogram and Blood Draw | ||
<1 year | 54 (47%) | |
1 to <2 years | 35 (30%) | |
2 to <3 years | 19 (16%) | |
3 to <4 years | 8 (7%) |
Chemical | All (n = 116) | Parous (n = 80) | Nulliparous (n = 36) | BMI (<25 kg/m2) (n = 56) | BMI (≥25 kg/m2) (n = 60) | |||||
---|---|---|---|---|---|---|---|---|---|---|
Beta ¶ (SE) | Padj † (p) § | Beta ¶ (SE) | Padj † (p) § | Beta ¶ (SE) | Padj † (p) § | Beta ¶ (SE) | Padj † (p) § | Beta ¶ (SE) | Padj † (p) § | |
PCB−138 | −0.81 (0.31) | 0.22 (0.010) | −0.78 (0.41) | >0.99 (0.060) | −0.94 (0.50) | >0.99 (0.068) | −1.02 (0.39) | 0.26 (0.011) | −0.33 (0.49) | >0.99 (0.50) |
PCB−153 | −0.87 (0.32) | 0.18 (0.008) | −0.79 (0.41) | >0.99 (0.059) | −1.10 (0.55) | >0.99 (0.053) | −0.58 (0.41) | >0.99 (0.17) | −1.22 (0.49) | 0.38 (0.016) |
PCB−203 | −0.60 (0.32) | >0.99 (0.062) | −0.78 (0.39) | >0.99 (0.049) | −0.08 (0.57) | >0.99 (0.90) | −0.12 (0.41) | >0.99 (0.77) | −1.12 (0.48) | 0.55 (0.024) |
PCB−74 | −0.53 (0.33) | >0.99 (0.11) | −0.99 (0.42) | >0.99 (0.020) | 0.32 (0.55) | >0.99 (0.56) | −0.75 (0.43) | >0.99 (0.084) | −0.23 (0.49) | >0.99 (0.64) |
PCB−187 | −0.45 (0.32) | >0.99 (0.16) | −0.38 (0.42) | >0.99 (0.37) | −0.67 (0.56) | >0.99 (0.24) | −0.01 (0.44) | >0.99 (0.97) | −1.12 (0.46) | 0.43 (0.019) |
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Lee, E.; Kinninger, A.; Ursin, G.; Tseng, C.; Hurley, S.; Wang, M.; Wang, Y.; Park, J.-S.; Petreas, M.; Deapen, D.; et al. Serum Levels of Commonly Detected Persistent Organic Pollutants and Per- and Polyfluoroalkyl Substances (PFASs) and Mammographic Density in Postmenopausal Women. Int. J. Environ. Res. Public Health 2020, 17, 606. https://doi.org/10.3390/ijerph17020606
Lee E, Kinninger A, Ursin G, Tseng C, Hurley S, Wang M, Wang Y, Park J-S, Petreas M, Deapen D, et al. Serum Levels of Commonly Detected Persistent Organic Pollutants and Per- and Polyfluoroalkyl Substances (PFASs) and Mammographic Density in Postmenopausal Women. International Journal of Environmental Research and Public Health. 2020; 17(2):606. https://doi.org/10.3390/ijerph17020606
Chicago/Turabian StyleLee, Eunjung, April Kinninger, Giske Ursin, Chiuchen Tseng, Susan Hurley, Miaomiao Wang, Yunzhu Wang, June-Soo Park, Myrto Petreas, Dennis Deapen, and et al. 2020. "Serum Levels of Commonly Detected Persistent Organic Pollutants and Per- and Polyfluoroalkyl Substances (PFASs) and Mammographic Density in Postmenopausal Women" International Journal of Environmental Research and Public Health 17, no. 2: 606. https://doi.org/10.3390/ijerph17020606