Phenotypic Dichotomy Following Developmental Exposure to Perfluorooctanoic Acid (PFOA) in Female CD-1 Mice: Low Doses Induce Elevated Serum Leptin and Insulin, and Overweight in Mid-life☆☆
Abstract
The synthetic surfactant, perfluorooctanoic acid (PFOA) is a proven developmental toxicant in mice, causing pregnancy loss, increased neonatal mortality, delayed eye opening, and abnormal mammary gland growth in animals exposed during fetal life. PFOA is found in the sera and tissues of wildlife and humans throughout the world, but is especially high in the sera of children compared to adults. These studies in CD-1 mice aim to determine the latent health effects of PFOA following: (1) an in utero exposure, (2) an in utero exposure followed by ovariectomy (ovx), or (3) exposure as an adult. Mice were exposed to 0, 0.01, 0.1, 0.3, 1, 3, or 5mg PFOA/kg BW for 17 days of pregnancy or as young adults. Body weight was reduced in the highest doses on postnatal day (PND) 1 and at weaning. However, the lowest exposures (0.01-0.3mg/kg) significantly increased body weight, and serum insulin and leptin (0.01-0.1mg/kg) in mid-life after developmental exposure. PFOA exposure combined with ovx caused no additional increase in mid-life body weight. At 18 months of age, the effects of in utero PFOA exposure on body weight were no longer detected. White adipose tissue and spleen weights were decreased at high doses of PFOA in intact developmentally exposed mice, and spleen weight was reduced in PFOA-exposed ovx mice. Brown adipose tissue weight was significantly increased in both ovx and intact mice at high PFOA doses. Liver weight was unaffected in late life by these exposure paradigms. Finally, there was no effect of adult exposure to PFOA on body weight. These studies demonstrate an important window of exposure for low-dose effects of PFOA on body weight gain, as well as leptin and insulin concentrations in mid-life, at a lowest observed effect level of 0.01mg PFOA/kg BW. The mode of action of these effects and its relevance to human health remain to be explored.
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The impacts of PFAS on body weight are not consistent in the literature, with many studies reporting associations between PFAS exposure and increased body weight gain and metabolic syndrome-like phenotypes in human and rodent studies.
“the impacts of PFAS on body weight are not consistent in the literature, with many studies reporting associations between PFAS exposure and increased body weight gain and metabolic syndrome-like phenotypes in human and rodent studies”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Hines et al., 2009
Cites
Serum Immunoreactive-Leptin Concentrations in Normal-Weight and Obese Humans
Considine, R. V., Sinha, M. K., Heiman, M. L., Kriauciunas, A., Stephens, T. W., Nyce, M. R., Ohannesian, J. P., Marco, C. C., McKee, L. J., Bauer, T. L., et al. (1996) · New England Journal of Medicine · doi:10.1056/nejm199602013340503 · Cited by 6,326 · see citing works
Perfluoroalkyl Acids: A Review of Monitoring and Toxicological Findings
Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., & Seed, J. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm128 · Cited by 2,620 · see citing works
Olsen, G. W., Burris, J. M., Ehresman, D. J., Froehlich, J. W., Seacat, A. M., Butenhoff, J. L., & Zobel, L. R. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10009 · Cited by 2,049 · see citing works
Calafat, A. M., Wong, L.-Y., Kuklenyik, Z., Reidy, J. A., & Needham, L. L. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10598 · Cited by 1,247 · see citing works
Carey, D., Jenkins, A. B., Campbell, L. V., Freund, J., & Chisholm, D. J. (1996) · Diabetes · doi:10.2337/diab.45.5.633 · Cited by 659 · see citing works
Perfluorinated Chemicals and Fetal Growth: A Study within the Danish National Birth Cohort
Fei, C., McLaughlin, J. K., Tarone, R. E., & Olsen, J. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10506 · Cited by 628 · see citing works
Apelberg, B. J., Witter, F. R., Herbstman, J. B., Calafat, A. M., Halden, R. U., Needham, L. L., & Goldman, L. R. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10334 · Cited by 619 · see citing works
Endocrine-Disrupting Organotin Compounds Are Potent Inducers of Adipogenesis in Vertebrates
Grün, F., Watanabe, H., Zamanian, Z., Maeda, L. S., Arima, K., Cubacha, R., Gardiner, D. M., Kanno, J., Iguchi, T., & Blumberg, B. (2006) · Molecular Endocrinology · doi:10.1210/me.2005-0367 · Cited by 612 · see citing works
Effects of perfluorooctanoic acid exposure during pregnancy in the mouse.
Lau, C., Thibodeaux, J. R., Hanson, R., Narotsky, M., Rogers, J. M., Lindstrom, A., & Strynar, M. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfj105 · Cited by 547 · see citing works
Inoue, K., Okada, F., Ito, R., Kato, S., Sasaki, S., 中島そのみ, Uno, A., Saijo, Y., Sata, F., Yoshimura, Y., et al. (2004) · Environmental Health Perspectives · doi:10.1289/ehp.6864 · Cited by 460 · see citing works
Takacs, M. L., & Abbott, B. D. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfl135 · Cited by 396 · see citing works
TOXICITY AND TOXICOKINETICS OF PERFLUOROOCTANOIC ACID IN HUMANS AND ANIMALS
KUDO, N., & KAWASHIMA, Y. (2003) · The Journal of Toxicological Sciences · doi:10.2131/jts.28.49 · Cited by 392 · see citing works
Emmett, E. A., Shofer, F. S., Zhang, H., Freeman, D. W., Desai, C. S., & Shaw, L. M. J. (2006) · Journal of Occupational and Environmental Medicine · doi:10.1097/01.jom.0000232486.07658.74 · Cited by 357 · see citing works
Hölzer, J., Midasch, O., Rauchfuss, K., Kraft, M., Reupert, R., Angerer, J., Kleeschulte, P., Marschall, N., & Wilhelm, M. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11064 · Cited by 356 · see citing works
Mechanisms of Extrahepatic Tumor Induction by Peroxisome Proliferators in Male CD Rats
Biegel, L. B., Hurtt, M. E., Frame, S. R., O’Connor, J. C., & Cook, J. C. (2001) · Toxicological Sciences · doi:10.1093/toxsci/60.1.44 · Cited by 349 · see citing works
Tissue distribution, metabolism, and elimination of perfluorooctanoic acid in male and female rats
Heuvel, J. P. V., Kuslikis, B. I., Rafelghem, M. J. V., & Peterson, R. E. (1991) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.2570060202 · Cited by 289 · see citing works
Harada, K. H., Inoue, K., Morikawa, A., Yoshinaga, T., Saito, N., & Koizumi, A. (2005) · Environmental Research · doi:10.1016/j.envres.2004.12.003 · Cited by 286 · see citing works
Miyawaki, J., Sakayama, K., Kato, H., Yamamoto, H., & Masuno, H. (2007) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.e486 · Cited by 282 · see citing works
Developmental exposure to endocrine disruptors and the obesity epidemic
Newbold, R. R., Padilla‐Banks, E., Snyder, R. J., Phillips, T. M., & Jefferson, W. N. (2007) · Reproductive Toxicology · doi:10.1016/j.reprotox.2006.12.010 · Cited by 276 · see citing works
Abbott, B. D., Wolf, C. J., Schmid, J., Das, K. P., ZEHR, R. D. J., Helfant, L., Nakayama, S. F., Lindstrom, A. B., Strynar, M. J., & Lau, C. S. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm110 · Cited by 262 · see citing works
White, S., Calafat, A., Kuklenyik, Z., Villanueva, L. R., Zehr, R. D., Helfant, L., Strynar, M., Lindstrom, A., Thibodeaux, J. R., Wood, C., et al. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfl177 · Cited by 229 · see citing works
Abbott, B. D. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.10.001 · Cited by 218 · see citing works
Kuklenyik, Z., Needham, L. L., & Calafat, A. M. (2005) · Analytical Chemistry · doi:10.1021/ac050671l · Cited by 203 · see citing works
Wolf, C. J., Fenton, S., Schmid, J., Calafat, A., Kuklenyik, Z., Bryant, X. A., Thibodeaux, J. R., Das, K., White, S., Lau, C., et al. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfl159 · Cited by 199 · see citing works
Medina‐Gómez, G., Gray, S. L., & Vidal‐Puig, A. (2007) · Public Health Nutrition · doi:10.1017/s1368980007000614 · Cited by 195 · see citing works
Relations between metabolic syndrome, oxidative stress and inflammation and cardiovascular disease.
Holvoet, P. (2008) · PubMed · Cited by 185 · see citing works
Olsen, G. W., Gilliland, F. D., Burlew, M., Burris, J. M., Mandel, J. S., & Mandel, J. H. (1998) · Journal of Occupational and Environmental Medicine · doi:10.1097/00043764-199807000-00006 · Cited by 169 · see citing works
Carey, D., Jenkins, A. B., Campbell, L. V., et al. (1996) · Diabetes · doi:10.2337/diabetes.45.5.633 · Cited by 154 · see citing works
Developmental exposure to estrogenic compounds and obesity
Newbold, R. R., Padilla‐Banks, E., Snyder, R. J., & Jefferson, W. N. (2005) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20147 · Cited by 132 · see citing works
Yang, Q., Xie, Y., Alexson, S. E. H., Dean Nelson, B., & DePierre, J. W. (2002) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)00923-1 · Cited by 131 · see citing works
Olsen, G. W., Church, T. R., Hansen, K. J., Burris, J. M., Butenhoff, J. L., Mandel, J. H., & Zobel, L. R. (2004) · Journal of Children s Health · doi:10.3109/15417060490447378 · Cited by 110 · see citing works
Perfluorooctanoate: Placental and lactational transport pharmacokinetics in rats.
Hinderliter, P., Mylchreest, E., Gannon, S. A., Butenhoff, J., & Kennedy, G. (2005) · Toxicology · doi:10.1016/j.tox.2005.03.010 · Cited by 101 · see citing works
Early Occurrence of Spontaneous Tumors in CD-1 Mice and Sprague—Dawley Rats
Son, W., & Gopinath, C. (2004) · Toxicologic Pathology · doi:10.1080/01926230490440871 · Cited by 96 · see citing works
White, S., Kato, K., Jia, L. T., Basden, B. J., Calafat, A., Hines, E., Stanko, J., Wolf, C. J., Abbott, B., & Fenton, S. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.11.054 · Cited by 88 · see citing works
Fenton, S., Reiner, J. L., Nakayama, S., Delinsky, A. D., Stanko, J., Hines, E., White, S., Lindstrom, A., Strynar, M., & Petropoulou, S.-S. E. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2009.02.012 · Cited by 80 · see citing works
Liu, R. C. M. (1996) · Fundamental and Applied Toxicology · doi:10.1006/faat.1996.0059 · Cited by 78 · see citing works
Montecucco, F., Steffens, S., & Mach, F. (2008) · Mediators of Inflammation · doi:10.1155/2008/767623 · Cited by 62 · see citing works
Xie, Y., Yang, Q., Nelson, B. D., & DePierre, J. W. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00386-1 · Cited by 55 · see citing works
Characterization of the adipose tissue atrophy induced by peroxisome proliferators in mice
Xie, Y., Yang, Q., Nelson, B. D., & DePierre, J. W. (2002) · Lipids · doi:10.1007/s11745-002-0873-7 · Cited by 36 · see citing works
Obesity in transgenic female mice with constitutively elevated luteinizing hormone secretion
Kero, J. T., Savontaus, E., Mikola, M., Pesonen, U., Koulu, M., Keri, R. A., Nilson, J. H., POUTANEN, M. H., & Huhtaniemi, I. T. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00367.2002 · Cited by 29 · see citing works
Lymphomas and High-Level Expression of Murine Leukemia Viruses in CFW Mice
Taddesse-Heath, L., Chattopadhyay, S. K., Dillehay, D. L., Lander, M. R., Nagashfar, Z., Morse, H. C., & Hartley, J. W. (2000) · Journal of Virology · doi:10.1128/jvi.74.15.6832-6837.2000 · Cited by 26 · see citing works
Increased beta-adrenergic receptors in brown fat of winter-acclimatized Alaskan voles
Feist, D. D. (1983) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1983.245.3.r357 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Fenton, S. E., Ducatman, A., Boobis, A., DeWitt, J. C., Lau, C., Ng, C., Smith, J. S., & Roberts, S. M. (2020) · Environmental Toxicology and Chemistry · doi:10.1002/etc.4890 · Cited by 2,445 · see citing works
EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals
Gore, A. C., Chappell, V. A., Fenton, S. E., Flaws, J. A., Nadal, A., Prins, G. S., Toppari, J., & Zoeller, R. T. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1010 · Cited by 2,407 · see citing works
Metabolism disrupting chemicals and metabolic disorders
Heindel, J. J., Blumberg, B., Cave, M., Machtinger, R., Mantovani, A., Mendez, M. A., Nadal, A., Palanza, P., Panzica, G., Sargis, R., et al. (2017) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.10.001 · Cited by 1,101 · see citing works
Risk to human health related to the presence of perfluoroalkyl substances in food
Panel), E. P. O. C. I. T. F. C. (. C., Schrenk, D., Bignami, M., Bodin, L., Chipman, J. K., del Mazo, J., Grasl‐Kraupp, B., Hogstrand, C., Hoogenboom, L. (., Leblanc, J., et al. (2020) · EFSA Journal · doi:10.2903/j.efsa.2020.6223 · Cited by 989 · see citing works
Endocrine Disruptors: From Endocrine to Metabolic Disruption
Casals-Casas, C., & Desvergne, B. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-012110-142200 · Cited by 902 · see citing works
Post, G. B., Cohn, P. D., & Cooper, K. R. (2012) · Environmental Research · doi:10.1016/j.envres.2012.03.007 · Cited by 639 · see citing works
Fluorinated Compounds in U.S. Fast Food Packaging
Schaider, L. A., Balan, S. A., Blum, A., Andrews, D. Q., Strynar, M. J., Dickinson, M. E., Lunderberg, D. M., Lang, J. R., & Peaslee, G. F. (2017) · Environmental Science & Technology Letters · doi:10.1021/acs.estlett.6b00435 · Cited by 620 · see citing works
Endocrine disrupters as obesogens
Grün, F., & Blumberg, B. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.02.018 · Cited by 586 · see citing works
Nelson, J. W., Hatch, E. E., & Webster, T. F. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.0901165 · Cited by 538 · see citing works
(CONTAM), E. P. O. C. I. T. F. C., Knutsen, H. K., Alexander, J., Barregård, L., Bignami, M., Brüschweiler, B. J., Ceccatelli, S., Cottrill, B., Dinovi, M., Edler, L., et al. (2018) · EFSA Journal · doi:10.2903/j.efsa.2018.5194 · Cited by 519 · see citing works
Blake, B. E., & Fenton, S. E. (2020) · Toxicology · doi:10.1016/j.tox.2020.152565 · Cited by 499 · see citing works
Johnson, P. I., Sutton, P., Atchley, D. S., Koustas, E., Lam, J., Sen, S., Robinson, K. A., Axelrad, D. A., & Woodruff, T. J. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307893 · Cited by 449 · see citing works
Endocrine disruptors and obesity
Heindel, J. J., Newbold, R. R., & Schug, T. T. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.163 · Cited by 429 · see citing works
Rappazzo, K., Coffman, E., & Hines, E. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14070691 · Cited by 405 · see citing works
Environmental Endocrine-Disrupting Chemical Exposure: Role in Non-Communicable Diseases
Kumar, M., Sarma, D. K., Shubham, S., Kumawat, M., Verma, V., Prakash, A., & Tiwari, R. R. (2020) · Frontiers in Public Health · doi:10.3389/fpubh.2020.553850 · Cited by 394 · see citing works
Toxicological Function of Adipose Tissue: Focus on Persistent Organic Pollutants
Merrill, M. A. L., Emond, C., Kim, M. J., Antignac, J., Bizec, B. L., Clément, K., Birnbaum, L. S., & Barouki, R. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1205485 · Cited by 372 · see citing works
Halldorsson, T. I., Rytter, D., Haug, L. S., Bech, B. H., Danielsen, I., Becher, G., Henriksen, T. B., & Olsen, S. F. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104034 · Cited by 353 · see citing works
Koustas, E., Lam, J., Sutton, P., Johnson, P. I., Atchley, D. S., Sen, S., Robinson, K. A., Axelrad, D. A., & Woodruff, T. J. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307177 · Cited by 349 · see citing works
Environmental Obesogens: Mechanisms and Controversies
Heindel, J. J., & Blumberg, B. (2018) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010818-021304 · Cited by 341 · see citing works
Rickard, B. P., Rizvi, I., & Fenton, S. E. (2022) · Toxicology · doi:10.1016/j.tox.2021.153031 · Cited by 334 · see citing works
Per- and polyfluorinated substances (PFASs): Environmental challenges
Krafft, M. P., & Riess, J. G. (2015) · Current Opinion in Colloid & Interface Science · doi:10.1016/j.cocis.2015.07.004 · Cited by 294 · see citing works
Endocrine disrupting properties of perfluorooctanoic acid,
White, S., Fenton, S., & Hines, E. (2011) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.03.011 · Cited by 295 · see citing works
Espartero, L. J. L., Yamada, M., Ford, J., Owens, G., Prow, T. W., & Juhasz, A. L. (2022) · Environmental Research · doi:10.1016/j.envres.2022.113431 · Cited by 282 · see citing works
Endocrine disrupting chemicals and the developmental programming of adipogenesis and obesity
Janesick, A., & Blumberg, B. (2011) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20197 · Cited by 269 · see citing works
Maisonet, M., Terrell, M. L., Mcgeehin, M., Christensen, K., Holmes, A. K., Calafat, A., & Marcus, M. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1003096 · Cited by 228 · see citing works
Blake, B. E., Pinney, S. M., Hines, E. P., Fenton, S. E., & Ferguson, K. K. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.07.042 · Cited by 236 · see citing works
Self-citationPrenatal Perfluoroalkyl Substance Exposure and Child Adiposity at 8 Years of Age: The HOME Study
Braun, J. M., Chen, A.-M., Romano, M., Calafat, A., Webster, G. M., Yolton, K., & Lanphear, B. (2015) · Obesity · doi:10.1002/oby.21258 · Cited by 223 · see citing works
Mastrantonio, M., Bai, E., Uccelli, R., Cordiano, V., Screpanti, A., & Crosignani, P. (2018) · European Journal of Public Health · doi:10.1093/eurpub/ckx066 · Cited by 228 · see citing works
Association of endocrine disruptors and obesity: perspectives from epidemiological studies
Hatch, E. E., Nelson, J. W., Stahlhut, R. W., & Webster, T. F. (2010) · International Journal of Andrology · doi:10.1111/j.1365-2605.2009.01035.x · Cited by 230 · see citing works
Endocrine-disrupting chemicals and the regulation of energy balance
Nadal, Á., Quesada, I., Tudurí, E., Nogueiras, R., & Alonso‐Magdalena, P. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2017.51 · Cited by 219 · see citing works
Parma consensus statement on metabolic disruptors
Heindel, J. J., Saal, F. S. V., Blumberg, B., Bovolin, P., Calamandrei, G., Ceresini, G., Cohn, B. A., Fabbri, E., Gioiosa, L., Kassotis, C. D., et al. (2015) · Environmental Health · doi:10.1186/s12940-015-0042-7 · Cited by 213 · see citing works
Predicting Later-Life Outcomes of Early-Life Exposures
Boekelheide, K., Blumberg, B., Chapin, R. E., Cote, I., Graziano, J. H., Janesick, A., Lane, R. H., Lillycrop, K. A., Myatt, L., States, J. C., et al. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1204934 · Cited by 200 · see citing works
Obesity II: Establishing causal links between chemical exposures and obesity
Heindel, J., Howard, S., Agay-Shay, K., Arrebola, J., Audouze, K., Babin, P. J., Barouki, R., Bansal, A., Blanc, E. B., Cave, M., et al. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.115015 · Cited by 173 · see citing works
Childhood Obesity and Environmental Chemicals
Merrill, M. A. L., & Birnbaum, L. S. (2011) · Mount Sinai Journal of Medicine A Journal of Translational and Personalized Medicine · doi:10.1002/msj.20229 · Cited by 192 · see citing works
Do Interactions Between Gut Ecology and Environmental Chemicals Contribute to Obesity and Diabetes?
Snedeker, S. M., & Hay, A. G. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1104204 · Cited by 184 · see citing works
Bastos Sales, L., Kamstra, J. H., Cenijn, P. H., van Rijt, L. S., Hamers, T., & Legler, J. (2013) · Toxicology in Vitro · doi:10.1016/j.tiv.2013.04.005 · Cited by 181 · see citing works
Prenatal Exposure to Perfluoroalkyl Substances and Adiposity in Early and Mid-Childhood
Mora, A. M., Oken, E., Rifas‐Shiman, S. L., Webster, T. F., Gillman, M. W., Calafat, A. M., Ye, X., & Sagiv, S. K. (2016) · Environmental Health Perspectives · doi:10.1289/ehp246 · Cited by 178 · see citing works
Perfluorinated Alkyl Substances
Grandjean, P., & Clapp, R. (2015) · NEW SOLUTIONS A Journal of Environmental and Occupational Health Policy · doi:10.1177/1048291115590506 · Cited by 181 · see citing works
Chen, Z., Yang, T., Walker, D. I., Thomas, D. C., Qiu, C., Chatzi, L., Alderete, T. L., Kim, J. S., Conti, D. V., Breton, C. V., et al. (2020) · Environment International · doi:10.1016/j.envint.2020.106091 · Cited by 176 · see citing works
Effects of Environmental Exposures on Fetal and Childhood Growth Trajectories
Zheng, T., Zhang, J., Sommer, K., Bassig, B. A., Zhang, X., Braun, J., Shuang-qing, X., Boyle, P., Zhang, B., Shi, K., et al. (2016) · Annals of Global Health · doi:10.1016/j.aogh.2016.01.008 · Cited by 174 · see citing works
Vagi, S. J., Azziz‐Baumgartner, E., Sjödin, A., Calafat, A. M., Dumesic, D. A., Gonzalez, L., Kato, K., Silva, M. J., Ye, X., & Azziz, R. (2014) · BMC Endocrine Disorders · doi:10.1186/1472-6823-14-86 · Cited by 169 · see citing works
Gorrochategui, E., Pérez-Albaladejo, E., Casas, J., Lacorte, S., & Porte, C. (2014) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2014.03.012 · Cited by 168 · see citing works
Starnes, H. M., Rock, K. D., Jackson, T. W., & Belcher, S. M. (2022) · Frontiers in Toxicology · doi:10.3389/ftox.2022.881584 · Cited by 166 · see citing works
Dietary Habits Related to Food Packaging and Population Exposure to PFASs
Susmann, H. P., Schaider, L. A., Rodgers, K. M., & Rudel, R. A. (2019) · Environmental Health Perspectives · doi:10.1289/ehp4092 · Cited by 165 · see citing works
Obesogens: An Environmental Link to Obesity
Holtcamp, W. N. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.120-a62 · Cited by 163 · see citing works
Alderete, T. L., Jin, R., Walker, D. I., Valvi, D., Chen, Z., Jones, D. P., Peng, C., Gilliland, F. D., Berhane, K. T., Conti, D. V., et al. (2019) · Environment International · doi:10.1016/j.envint.2019.02.047 · Cited by 159 · see citing works
Santander, N. M., Valvi, D., López-Espinosa, M.-J., Manzano-Salgado, C. B., Ballester, F., Ibarluzea, J. M., Santa‐Marina, L., Schettgen, T., Guxens, M., Sunyer, J., et al. (2017) · Environmental Health Perspectives · doi:10.1289/ehp1062 · Cited by 159 · see citing works
Borg, D., Lund, B.-O., Lindquist, N.-G., & Håkansson, H. (2013) · Environment International · doi:10.1016/j.envint.2013.05.009 · Cited by 155 · see citing works
Post, G. B., Louis, J. B., Cooper, K. R., Boros-Russo, B. J., & Lippincott, R. L. (2009) · Environmental Science & Technology · doi:10.1021/es900301s · Cited by 155 · see citing works
Negri, E., Metruccio, F., Guercio, V., Tosti, L., Benfenati, E., Bonzi, R., la Vecchia, C., & Moretto, A. (2017) · Critical Reviews in Toxicology · doi:10.1080/10408444.2016.1271972 · Cited by 127 · see citing works
Tsai, M., Lin, C., Lin, C., Chen, M., Hsu, S. H.-J., Chien, K., Sung, F., Chen, P., & Su, T. (2015) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2015.03.008 · Cited by 134 · see citing works
Hanssen, L., Röllin, H. B., Odland, J. Ø., Moe, M. K., & Sandanger, T. M. (2010) · Journal of Environmental Monitoring · doi:10.1039/b924420d · Cited by 132 · see citing works
Endocrine disrupting chemicals in mixture and obesity, diabetes and related metabolic disorders
Magueresse‐Battistoni, B. L., Labaronne, E., Vidal, H., & Naville, D. (2017) · World Journal of Biological Chemistry · doi:10.4331/wjbc.v8.i2.108 · Cited by 123 · see citing works
Seals, R. M., Bartell, S. M., & Steenland, K. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1002346 · Cited by 123 · see citing works
Adipocytes under assault: Environmental disruption of adipose physiology
Regnier, S. M., & Sargis, R. M. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.05.028 · Cited by 121 · see citing works
Dalsager, L., Christensen, N., Husby, S., Kyhl, H. B., Nielsen, F., Høst, A., Grandjean, P., & Jensen, T. K. (2016) · Environment International · doi:10.1016/j.envint.2016.08.026 · Cited by 119 · see citing works
Tucker, D. K., Bouknight, S. H., Brar, S. S., Kissling, G. E., & Fenton, S. E. (2018) · Environmental Health Perspectives · doi:10.1289/ehp3189 · Cited by 117 · see citing works
The effects of perfluorinated chemicals on adipocyte differentiation in vitro
Watkins, A. M., Wood, C. R., Lin, M. T., & Abbott, B. D. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.10.020 · Cited by 116 · see citing works
Karlsen, M., Grandjean, P., Weihe, P., Steuerwald, U., Oulhote, Y., & Valvi, D. (2016) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.08.002 · Cited by 113 · see citing works
Valsecchi, S. M., Conti, D., Crebelli, R., Polesello, S., Rusconi, M., Mazzoni, M., Preziosi, E., Carere, M., Lucentini, L., Ferretti, E., et al. (2016) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2016.04.055 · Cited by 112 · see citing works
Macon, M. B., Villanueva, L. R., Tatum-Gibbs, K. R., ZEHR, R. D. J., Strynar, M. J., Stanko, J. P., White, S. S., Helfant, L., & Fenton, S. E. (2011) · Toxicological Sciences · doi:10.1093/toxsci/kfr076 · Cited by 110 · see citing works
Endocrine disruption and obesity: A current review on environmental obesogens
Gupta, R., Kumar, P., Fahmi, N., Garg, B., Dutta, S., Sachar, S., Matharu, A. S., & Vimaleswaran, K. S. (2020) · Current Research in Green and Sustainable Chemistry · doi:10.1016/j.crgsc.2020.06.002 · Cited by 108 · see citing works
Høyer, B. B., Ramlau‐Hansen, C. H., Vrijheid, M., Valvi, D., Pedersen, H. S., Zviezdai, V., Jönsson, B., Lindh, C. H., Bonde, J. ., & Toft, G. V. (2015) · Environmental Health Perspectives · doi:10.1289/ehp.1408881 · Cited by 107 · see citing works
Prenatal Exposures to Perfluorinated Chemicals and Anthropometry at 7 Years of Age
Andersen, C. S., Fei, C., Gamborg, M., Nohr, E. A., Sørensen, T. I. A., & Olsen, J. (2013) · American Journal of Epidemiology · doi:10.1093/aje/kwt057 · Cited by 108 · see citing works
Lau, C. S. (2012) · Proceedings of the Fourth International Symposium on Polarization Phenomena in Nuclear Reactions · doi:10.1007/978-3-7643-8340-4_3 · Cited by 103 · see citing works
Koskela, A., Finnilä, M., Korkalainen, M., Spulber, S. D., Koponen, J. M., Håkansson, H., Tuukkanen, J., & Viluksela, M. (2016) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2016.04.002 · Cited by 101 · see citing works
Manzano-Salgado, C. B., Casas, M., López-Espinosa, M.-J., Ballester, F., Íñiguez, C., Martinez, D. R., Romaguera, D., Fernández‐Barrés, S., Santa‐Marina, L., Basterretxea, M., et al. (2017) · Environmental Health Perspectives · doi:10.1289/ehp1330 · Cited by 100 · see citing works
Rich, C. D., Blaine, A. C., Hundal, L. S., & Higgins, C. P. (2014) · Environmental Science & Technology · doi:10.1021/es504152d · Cited by 95 · see citing works
Developmental origins of obesity and type 2 diabetes: molecular aspects and role of chemicals
Inadera, H. (2013) · Environmental Health and Preventive Medicine · doi:10.1007/s12199-013-0328-8 · Cited by 100 · see citing works
Obesity and endocrine-disrupting chemicals
Amato, A. A., Wheeler, H. B., & Blumberg, B. (2021) · Endocrine Connections · doi:10.1530/ec-20-0578 · Cited by 103 · see citing works
Goodrich, J. A., Walker, D. I., He, J., Lin, X., Baumert, B. O., Hu, X., Alderete, T. L., Chen, Z., Valvi, D., Fuentes, Z. C., et al. (2023) · Environmental Health Perspectives · doi:10.1289/ehp11372 · Cited by 96 · see citing works
Guthman, J. (2012) · Annals of the Association of American Geographers · doi:10.1080/00045608.2012.659635 · Cited by 95 · see citing works
Filgo, A. J., Quist, E. M., Hoenerhoff, M. J., Brix, A. E., Kissling, G. E., & Fenton, S. E. (2014) · Toxicologic Pathology · doi:10.1177/0192623314558463 · Cited by 93 · see citing works
Stratakis, N., Rock, S., Merrill, M. A. L., Sáez, M., Robinson, O., Fecht, D., Vrijheid, M., Valvi, D., Conti, D. V., McConnell, R., et al. (2021) · Obesity Reviews · doi:10.1111/obr.13383 · Cited by 94 · see citing works
Early-life exposure to perfluoroalkyl substances and childhood metabolic function
Fleisch, A. F., Rifas-Shiman, S. L., Mora, A. M., Calafat, A. M., Ye, X., Luttmann-Gibson, H., Gillman, M. W., Oken, E., & Sagiv, S. K. (2017) · Environmental Health Perspectives · doi:10.1289/ehp303 · Cited by 91 · see citing works
Prenatal Exposure to Perfluoroalkyl Substances: Infant Birth Weight and Early Life Growth
Shoaff, J., Papandonatos, G., Calafat, A., Chen, A.-M., Lanphear, B., Ehrlich, S., Kelsey, K., & Braun, J. (2018) · Environmental Epidemiology · doi:10.1097/ee9.0000000000000010 · Cited by 73 · see citing works
The obesogenic effect of high fructose exposure during early development
Goran, M. I., Dumke, K. A., Bouret, S. G., Kayser, B. D., Walker, R. W., & Blumberg, B. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.108 · Cited by 90 · see citing works
PFAS and Potential Adverse Effects on Bone and Adipose Tissue through Interactions with PPARγ
Kirk, A. B., Michelsen-Correa, S., Rosen, C., Martin, C. F., & Blumberg, B. (2021) · Endocrinology · doi:10.1210/endocr/bqab194 · Cited by 90 · see citing works
Perfluorinated Compounds: An Overview
Lau, C. S. (2015) · Molecular and integrative toxicology · doi:10.1007/978-3-319-15518-0_1 · Cited by 86 · see citing works
Guo, H., Wang, J., Yao, J., Sun, S., Sheng, N., Zhang, X., Guo, X., Guo, Y., Sun, Y., & Dai, J. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b00148 · Cited by 83 · see citing works
Obesogenic effects of endocrine disruptors, what do we know from animal and human studies?
de Cock, M., & van de Bor, M. (2014) · Environment International · doi:10.1016/j.envint.2014.04.022 · Cited by 82 · see citing works
Peng, B.-X., Li, F., Mortimer, M., Xiao, X., Ni, Y., Lei, Y., Li, M., & Guo, L. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.157313 · Cited by 81 · see citing works
Fenton, S., Reiner, J. L., Nakayama, S., Delinsky, A. D., Stanko, J., Hines, E., White, S., Lindstrom, A., Strynar, M., & Petropoulou, S.-S. E. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2009.02.012 · Cited by 80 · see citing works
Persistent Organic Pollutants as Risk Factors for Obesity and Diabetes
Yang, C., Kong, A. P. S., Cai, Z., & Chung, A. C. K. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0966-0 · Cited by 81 · see citing works
Polluted Pathways: Mechanisms of Metabolic Disruption by Endocrine Disrupting Chemicals
Mimoto, M. S., Nadal, Á., & Sargis, R. M. (2017) · Current Environmental Health Reports · doi:10.1007/s40572-017-0137-0 · Cited by 78 · see citing works
Transgenerational inheritance of prenatal obesogen exposure
Janesick, A. S., Shioda, T., & Blumberg, B. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.09.002 · Cited by 76 · see citing works
Gui, S., Qiao, J.-C., Xu, K., Li, Z., Chen, Y.-N., Wu, K., Jiang, Z., & Hu, C. (2022) · Journal of Exposure Science & Environmental Epidemiology · doi:10.1038/s41370-022-00464-3 · Cited by 78 · see citing works
Li, X., Pham, H., Janesick, A., & Blumberg, B. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1205383 · Cited by 76 · see citing works
Gui, S.-Y., Chen, Y.-N., Wu, K.-J., Liu, W., Wang, W.-J., Liang, H.-R., Jiang, Z.-X., Li, Z.-L., & Hu, C.-Y. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.855348 · Cited by 80 · see citing works
Starling, A., Adgate, J., Hamman, R., Kechris, K., Calafat, A., & Dabelea, D. (2019) · Environment International · doi:10.1016/j.envint.2019.104983 · Cited by 67 · see citing works
Han, X., Meng, L., Zhang, G., Li, Y., Shi, Y., Zhang, Q., & Jiang, G. (2021) · Environment International · doi:10.1016/j.envint.2021.106637 · Cited by 74 · see citing works
Perfluorooctanoic acid exposure triggers oxidative stress in the mouse pancreas
Kamendulis, L. M., Wu, Q., Sandusky, G. E., & Hocevar, B. A. (2014) · Toxicology Reports · doi:10.1016/j.toxrep.2014.07.015 · Cited by 73 · see citing works
The impact of prenatal perfluoroalkyl substances exposure on neonatal and child growth.
Chen, M.-H., Ng, S., Hsieh, C.-J., Lin, C.-C., Hsieh, W. S., & Chen, P.-C. (2017) · Science of the Total Environment · doi:10.1016/j.scitotenv.2017.06.273 · Cited by 55 · see citing works
Childhood Ingestions of Environmental Toxins: What Are the Risks?
Hauptman, M., & Woolf, A. D. (2017) · Pediatric Annals · doi:10.3928/19382359-20171116-01 · Cited by 73 · see citing works
Tian, Y., Zeng, X., Bloom, M. S., Lin, S., Wang, S.-Q., Yim, S. H. L., Yang, M., Chu, C., Gurram, N., Hu, L., et al. (2019) · Environment International · doi:10.1016/j.envint.2019.01.006 · Cited by 73 · see citing works
Qin, W.-P., Cao, L.-Y., Li, C.-H., Guo, L.-H., Colbourne, J., & Ren, X.-M. (2020) · Environmental Science & Technology · doi:10.1021/acs.est.9b07295 · Cited by 71 · see citing works
Incidence of type II diabetes in a cohort with substantial exposure to perfluorooctanoic acid
Karnes, C., Winquist, A. G., & Steenland, K. (2013) · Environmental Research · doi:10.1016/j.envres.2013.11.003 · Cited by 71 · see citing works
PPAR α in Obesity: Sex Difference and Estrogen Involvement
Yoon, M. (2010) · PPAR Research · doi:10.1155/2010/584296 · Cited by 71 · see citing works
Liu, X., Zhang, L., Chen, L., Li, J., Wang, Y., Wang, J., Meng, G., Chi, M., Zhao, Y., Chen, H., et al. (2019) · Environment International · doi:10.1016/j.envint.2019.03.035 · Cited by 69 · see citing works
Braun, J. M., Eliot, M., Papandonatos, G. D., Buckley, J. P., Cecil, K. M., Kalkwarf, H. J., Chen, A., Eaton, C. B., Kelsey, K., Lanphear, B. P., et al. (2021) · International Journal of Obesity · doi:10.1038/s41366-020-00717-x · Cited by 67 · see citing works
- Authors
- Hines, E. P., White, S. S., Stanko, J. P., Gibbs-Flournoy, E. A., Lau, C., & Fenton, S. E.
- Affiliations
- Environmental Protection Agency (US)
- University of North Carolina at Chapel Hill (US)
- Venue
- Molecular and Cellular Endocrinology
- Publisher
- Elsevier BV
- Published
- 2009-05-25
- Volume
- 304
- Issue
- 1-2
- Pages
- 97-105
- ISSN
- 0303-7207 (ISSN-L)
- OpenAlex
- W2030560074
- Cited by
- 282
- References
- 41
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 12 · 2023: 21 · 2022: 24 · 2021: 27 · 2020: 21 · 2019: 18 · 2018: 13 · 2017: 23 · 2016: 17 · 2015: 16 · 2014: 20 · 2013: 15 · 2012: 13
- FWCI
- 9.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular and Cellular Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
- Keywords
- perfluorooctanoic acid, developmental toxicity, prenatal exposure, low-dose effects, leptin, insulin, weight gain, midlife, ovariectomy, brown adipose tissue, white adipose tissue, spleen weight, liver weight, ICR mice, perfluorinated compounds, endocrine disruption
- MeSH terms
- Animals, Body Weight, Caprylates, Female, Fluorocarbons, Humans, Insulin, Organ Size, Ovariectomy, Phenotype, Pregnancy, Prenatal Exposure Delayed Effects, Random Allocation, Maternal Exposure, Leptin, Overweight, Mice
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