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Original Articles

An overview of recent studies on the potential of pulp‐mill effluents to alter reproductive parameters in fish

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Pages 347-371 | Published online: 02 Sep 2009

Keep up to date with the latest research on this topic with citation updates for this article.

Read on this site (9)

KellyR. Munkittrick . (2009) Ubiquitous Criticisms of Ecological Field Studies. Human and Ecological Risk Assessment: An International Journal 15:4, pages 647-650.
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L. Mark Hewitt, JoanneL. Parrott & MarkE. McMaster. (2006) A Decade of Research on the Environmental Impacts of Pulp and Paper Mill Effluents in Canada: Sources and Characteristics of Bioactive Substances. Journal of Toxicology and Environmental Health, Part B 9:4, pages 341-356.
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MarkE. McMaster, L. Mark Hewitt & JoanneL. Parrott. (2006) A Decade of Research on the Environmental Impacts of Pulp and Paper Mill Effluents in Canada: Field Studies and Mechanistic Research. Journal of Toxicology and Environmental Health, Part B 9:4, pages 319-339.
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Ken D. Oakes, L. Mark Hewitt, Mark E. McMaster, Craig Wood, Kelly R. Munkittrick & Glen J. Van Der Kraak. (2005) Oxidative Stress and Sex Steroid Levels in Fish Following Short-Term Exposure to Pulp-Mill Effluents. Journal of Toxicology and Environmental Health, Part A 68:4, pages 267-286.
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Anders Svenson, Ann-Sofie Allard, Christian Junestedt, Olof Cerne & Mats Ek. (2004) Assessment of Androgenicity in Leachates from Swedish Landfills and Treatments for its Elimination. Journal of Environmental Science and Health, Part A 39:11-12, pages 2817-2825.
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Anders Svenson & Ann-Sofie Allard. (2004) Occurrence and Some Properties of the Androgenic Activity in Municipal Sewage Effluents. Journal of Environmental Science and Health, Part A 39:3, pages 693-701.
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Jeanette Rotchell & Gary Ostrander. (2003) Molecular Markers of Endocrine Disruption in Aquatic Organisms. Journal of Toxicology and Environmental Health, Part B 6:5, pages 453-496.
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Reynaldo Patiño, StevenL. Goodbred, Rassa Draugelis-Dale, CatherineE. Barry, J. Scott Foott, MelodyR. Wainscott, TimothyS. Gross & KennethJ. Covay. (2003) Morphometric and Histopathological Parameters of Gonadal Development in Adult Common Carp from Contaminated and Reference Sites in Lake Mead, Nevada. Journal of Aquatic Animal Health 15:1, pages 55-68.
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Seung Jun Kwack, Oran Kwon, Hyung Sik Kim, Soon Sun Kim, So Hee Kim, Kyung Hee Sohn, Rhee Da Lee, Chul Hoon Park, Eui Bae Jeung, Beum-Soo An & Kui Lea Park. (2002) COMPARATIVE EVALUATION OF ALKYLPHENOLIC COMPOUNDS ON ESTROGENIC ACTIVITY IN VITRO AND IN VIVO. Journal of Toxicology and Environmental Health, Part A 65:5-6, pages 419-431.
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Erin J. Ussery, Mark E. McMaster, Mark R. Servos, David H. Miller & Kelly R. Munkittrick. (2021) A 30-Year Study of Impacts, Recovery, and Development of Critical Effect Sizes for Endocrine Disruption in White Sucker (Catostomus commersonii) Exposed to Bleached-Kraft Pulp Mill Effluent at Jackfish Bay, Ontario, Canada. Frontiers in Endocrinology 12.
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T.J. Arciszewski, M.E. McMaster & K.R. Munkittrick. (2020) Long‐Term Studies of Fish Health before and after the Closure of a Bleached Kraft Pulp Mill in Northern Ontario, Canada. Environmental Toxicology and Chemistry 40:1, pages 162-176.
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Daniel Bernet, Thomas Wahli, Christoph Küng & Helmut Segner. (2020) Zooplankton Feeding Induces Macroscopical Gonad Malformations in Whitefish (Coregonus ssp.) from Lake Thun, Switzerland. Fishes 5:3, pages 26.
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Christopher J. Martyniuk, April Feswick, Kelly R. Munkittrick, David A. Dreier & Nancy D. Denslow. (2020) Twenty years of transcriptomics, 17alpha-ethinylestradiol, and fish. General and Comparative Endocrinology 286, pages 113325.
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Vicki S. Blazer, Heather L. Walsh, Cassidy H. Shaw, Luke R. Iwanowicz, Ryan P. Braham & Patricia M. Mazik. (2018) Indicators of exposure to estrogenic compounds at Great Lakes Areas of Concern: species and site comparisons. Environmental Monitoring and Assessment 190:10.
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Allisson Jhonatan Gomes Castro, Ivana Eunice Baptista, Kieiv Resende Sousa de Moura, Fernanda Padilha, Juliana Tonietto, Ariane Zamoner Pacheco de Souza, Carlos Henrique Lemos Soares, Fátima Regina Mena Barreto Silva & Glen Van Der Kraak. (2018) Exposure to a Brazilian pulp mill effluent impacts the testis and liver in the zebrafish. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 206-207, pages 41-47.
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Rodrigo Orrego, Craig B. Milestone, L. Mark Hewitt, John Guchardi, Tatiana Heid-Furley, Alison Slade, Deborah L. MacLatchy & Douglas Holdway. (2017) Evaluating the potential of effluent extracts from pulp and paper mills in Canada, Brazil, and New Zealand to affect fish reproduction: Estrogenic effects in fish. Environmental Toxicology and Chemistry 36:6, pages 1547-1555.
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Barbora Jarošová, Jakub Javůrek, Ondřej Adamovský & Klára Hilscherová. (2015) Phytoestrogens and mycoestrogens in surface waters — Their sources, occurrence, and potential contribution to estrogenic activity. Environment International 81, pages 26-44.
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Petra C. Lindholm-Lehto, Juha S. Knuutinen, Heidi S. J. Ahkola & Sirpa H. Herve. (2015) Refractory organic pollutants and toxicity in pulp and paper mill wastewaters. Environmental Science and Pollution Research 22:9, pages 6473-6499.
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Andrew Waye, Wudu E Lado, Pierre H Martel, John T Arnason & Vance L Trudeau. (2014) Ovulation but not milt production is inhibited in fathead minnows (Pimephales promelas) exposed to a reproductively inhibitory pulp mill effluent. Reproductive Biology and Endocrinology 12:1.
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April Feswick, Gerald T. Ankley, Nancy Denslow, Laura E. Ellestad, Meghan Fuzzen, Kathleen M. Jensen, Kevin Kroll, Andrea Lister, Deborah L. MacLatchy, Mark E. McMaster, Edward F. Orlando, Mark R. Servos, Gerald R. Tetreault, Michael R. Van Den Heuvel & Kelly R. Munkittrick. (2014) An inter-laboratory study on the variability in measured concentrations of 17β-estradiol, testosterone, and 11-ketotestosterone in white sucker: Implications and recommendations. Environmental Toxicology and Chemistry 33:4, pages 847-857.
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David KreutzweiserFrederick BeallKara WebsterDean ThompsonIrena Creed. (2013) Impacts and prognosis of natural resource development on aquatic biodiversity in Canada’s boreal zone. Environmental Reviews 21:4, pages 227-259.
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Claudio Salazar, Ignasi Sirés, Claudio A. Zaror & Enric Brillas. (2013) Treatment of a Mixture of Chloromethoxyphenols in Hypochlorite Medium by Electrochemical AOPs as an Alternative for the Remediation of Pulp and Paper Mill Process Waters. Electrocatalysis 4:4, pages 212-223.
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Anil K. Tyor, A. Fulia & R.K. Sharma. (2012) Anomalies in Cyprinus carpio Larvae Exposed to Paper Mill Effluent. Journal of Biological Sciences 12:5, pages 321-326.
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Tisha C. King-Heiden, Vatsal Mehta, Kong M. Xiong, Kevin A. Lanham, Dagmara S. Antkiewicz, Alissa Ganser, Warren Heideman & Richard E. Peterson. (2012) Reproductive and developmental toxicity of dioxin in fish. Molecular and Cellular Endocrinology 354:1-2, pages 121-138.
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Barry F. Mower, Kelly R. Munkittrick, Mark E. McMaster & Rebecca J. Van Beneden. (2011) Response of white sucker (Catostomus commersoni) to pulp and paper mill effluent in the Androscoggin River, Maine, USA. Environmental Toxicology and Chemistry 30:1, pages 142-153.
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Tisha C. King Heiden, Craig A. Struble, Matthew L. Rise, Martin J. Hessner, Reinhold J. Hutz & Michael J. CarvanIIIIII. (2008) Molecular targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) within the zebrafish ovary: Insights into TCDD-induced endocrine disruption and reproductive toxicity. Reproductive Toxicology 25:1, pages 47-57.
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M.S. PollockL.M.J. ClarkeM.G. Dubé. (2007) The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environmental Reviews 15:NA, pages 1-14.
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Edward F. Orlando & Louis J. GuilletteJr.Jr.. (2007) Sexual dimorphic responses in wildlife exposed to endocrine disrupting chemicals. Environmental Research 104:1, pages 163-173.
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Kevin S. Shaughnessy, Andrew M. Belknap, L. Mark Hewitt, Monique G. Dubé & Deborah L. MacLatchy. (2007) Effects of kraft pulp mill condensates on plasma testosterone levels in mummichog (Fundulus heteroclitus). Ecotoxicology and Environmental Safety 67:1, pages 140-148.
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Inga Christianson-Heiska, Pia Smeds, Nina Granholm, Eija Bergelin & Boris Isomaa. (2007) Endocrine modulating actions of a phytosterol mixture and its oxidation products in zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 145:4, pages 518-527.
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Nancy Denslow & Maria Sepúlveda. 2007. The Fish Oocyte. The Fish Oocyte 255 322 .
Andrew M. Belknap, Keith R. Solomon, Deborah L. MacLatchy, Monique G. Dubé & L. Mark Hewitt. (2009) Identification of compounds associated with testosterone depressions in fish exposed to bleached kraft pulp and paper mill chemical recovery condensates. Environmental Toxicology and Chemistry 25:9, pages 2322-2333.
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Carrie J. Rickwood, Monique G. Dubé, L. Mark Hewitt, Tibor G. Kovacs, Joanne L. Parrott & Deborah L. MacLatchy. (2009) Use of paired fathead minnow ( Pimephales promelas ) reproductive test. Part 1: Assessing biological effects of final bleached kraft pulp mill effluent using a mobile bioassay trailer system . Environmental Toxicology and Chemistry 25:7, pages 1836-1846.
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Alexander P. Scott, Ioanna Katsiadaki, Mark F. Kirby & John Thain. (2006) Relationship between Sex Steroid and Vitellogenin Concentrations in Flounder ( Platichthys flesus ) Sampled from an Estuary Contaminated with Estrogenic Endocrine-Disrupting Compounds . Environmental Health Perspectives 114:Suppl 1, pages 27-31.
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Tisha King Heiden, Michael J. CarvanIIIIII & Reinhold J. Hutz. (2006) Inhibition of Follicular Development, Vitellogenesis, and Serum 17β-Estradiol Concentrations in Zebrafish Following Chronic, Sublethal Dietary Exposure to 2,3,7,8-Tetrachlorodibenzo-p-Dioxin. Toxicological Sciences 90:2, pages 490-499.
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Katherine E. Liney, Susan Jobling, Jan A. Shears, Peter Simpson & Charles R. Tyler. (2005) Assessing the Sensitivity of Different Life Stages for Sexual Disruption in Roach ( Rutilus rutilus ) Exposed to Effluents from Wastewater Treatment Works . Environmental Health Perspectives 113:10, pages 1299-1307.
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Hiroshi Ishibashi, Naoko Watanabe, Naomi Matsumura, Masashi Hirano, Yukiko Nagao, Hideki Shiratsuchi, Shinya Kohra, Shin-ichi Yoshihara & Koji Arizono. (2005) Toxicity to early life stages and an estrogenic effect of a bisphenol A metabolite, 4-methyl-2,4-bis(4-hydroxyphenyl)pent-1-ene on the medaka (Oryzias latipes). Life Sciences 77:21, pages 2643-2655.
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Ken D. Oakes, Louis A. Tremblay & Glen J. Van Der Kraak. (2009) Short‐term lab exposures of immature rainbow trout ( Oncorhynchus mykiss ) to sulfite and kraft pulp‐mill effluents: Effects on oxidative stress and circulating sex steroids . Environmental Toxicology and Chemistry 24:6, pages 1451-1461.
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Lesley J. Mills & Clinton Chichester. (2005) Review of evidence: Are endocrine-disrupting chemicals in the aquatic environment impacting fish populations?. Science of The Total Environment 343:1-3, pages 1-34.
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L. Mark Hewitt & Chris H. Marvin. (2005) Analytical methods in environmental effects-directed investigations of effluents. Mutation Research/Reviews in Mutation Research 589:3, pages 208-232.
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C. R. Tyler, C. Spary, R. Gibson, E. M. Santos, J. Shears & E. M. Hill. (2005) Accounting for Differences in Estrogenic Responses in Rainbow Trout ( Oncorhynchus mykiss :  Salmonidae) and Roach ( Rutilus rutilus :  Cyprinidae) Exposed to Effluents from Wastewater Treatment Works . Environmental Science & Technology 39:8, pages 2599-2607.
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Akemi Yamaguchi, Hiroshi Ishibashi, Shinya Kohra, Koji Arizono & Nobuaki Tominaga. (2005) Short-term effects of endocrine-disrupting chemicals on the expression of estrogen-responsive genes in male medaka (Oryzias latipes). Aquatic Toxicology 72:3, pages 239-249.
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Helmut Segner. (2005) Developmental, Reproductive, and Demographic Alterations in Aquatic Wildlife: Establishing Causality between Exposure to Endocrine-active Compounds (EACs) and Effects. Acta hydrochimica et hydrobiologica 33:1, pages 17-26.
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Yuuki Tamagawa, Hirofumi Hirai, Shingo Kawai & Tomoaki Nishida. (2005) Removal of estrogenic activity of endocrine-disrupting genistein by ligninolytic enzymes from white rot fungi. FEMS Microbiology Letters 244:1, pages 93-98.
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Antony W. Wood, David M. Janz & Glen J. Van Der Kraak. 2005. Environmental Toxicology. Environmental Toxicology 303 328 .
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Anders Svenson & Ann‐Sofie Allard. (2004) In vitro androgenicity in pulp and paper mill effluents . Environmental Toxicology 19:5, pages 510-517.
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Tanu Rana, Shashank Gupta, Dhiraj Kumar, Sharad Sharma, Manish Rana, Vikram S Rathore & Ben M.J Pereira. (2004) Toxic effects of pulp and paper-mill effluents on male reproductive organs and some systemic parameters in rats. Environmental Toxicology and Pharmacology 18:1, pages 1-7.
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Kimberley A Gilbride & Roberta R Fulthorpe. (2004) A survey of the composition and diversity of bacterial populations in bleached kraft pulp-mill wastewater secondary treatment systems. Canadian Journal of Microbiology 50:8, pages 633-644.
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Nancy D Denslow, Jannet Kocerha, Maria S Sepúlveda, Timothy Gross & Stewart E Holm. (2004) Gene expression fingerprints of largemouth bass (Micropterus salmoides) exposed to pulp and paper mill effluents. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 552:1-2, pages 19-34.
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K. R. Munkittrick. 2004. Fishes and Forestry. Fishes and Forestry 336 361 .
Ann Oliver Cheek, V. William King, Jeanine R. Burse, Dennis L. Borton & Craig V. Sullivan. (2004) Bluegill (Lepomis macrochirus) vitellogenin: purification and enzyme-linked immunosorbent assay for detection of endocrine disruption by papermill effluent. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 137:3, pages 249-260.
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R. van Aerle, T. J. Runnalls & C. R. Tyler. (2004) Ontogeny of gonadal sex development relative to growth in fathead minnow. Journal of Fish Biology 64:2, pages 355-369.
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Hiroshi Ishibashi, Makito Kobayashi, Yuki Tomiyasu, Maki Miyahara, Katsuyasu Tachibana, Mutsuyosi Tsuchimoto & Koji Arizono. (2004) Development of Plasma Vitellogenin Assay for Estrogenic Effects of Endocrine-Disrupting Chemicals Using Ovariectomized Goldfish (Carassius auratus). Journal of Health Science 50:2, pages 169-173.
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Frédéric D.L. Leusch & Deborah L. MacLatchy. (2003) In vivo implants of β-sitosterol cause reductions of reactive cholesterol pools in mitochondria isolated from gonads of male goldfish (Carassius auratus). General and Comparative Endocrinology 134:3, pages 255-263.
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Dorothy Thornton, Robert A. Kagan & Neil Gunningham. (2003) Sources of Corporate Environmental Performance. California Management Review 46:1, pages 127-141.
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Yiannis Kiparissis, Gordon C Balch, Tracy L Metcalfe & Chris D Metcalfe. (2003) Effects of the isoflavones genistein and equol on the gonadal development of Japanese medaka Oryzias latipes.. Environmental Health Perspectives 111:9, pages 1158-1163.
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Ken D. Oakes & Glen J. Van Der Kraak. (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquatic Toxicology 63:4, pages 447-463.
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S. JOBLING & C. R. TYLER. (2003) Endocrine disruption, parasites and pollutants in wild freshwater fish. Parasitology 126:7, pages S103-S107.
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A.C Pryce-Hobby, M.E McMaster, L.M Hewitt & G Van Der Kraak. (2003) The effects of pulp mill effluent on the sex steroid binding protein in white sucker (Catostomus commersoni) and longnose sucker (C. catostomus). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 134:2, pages 241-250.
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Christine I. Gilman, Frederic D.L. Leusch, W. Carl Breckenridge & Deborah L. MacLatchy. (2003) Effects of a phytosterol mixture on male fish plasma lipoprotein fractions and testis P450scc activity. General and Comparative Endocrinology 130:2, pages 172-184.
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Yasushi Kamaya, Yasunori Kurogi & Kyoji Suzuki. (2003) Acute toxicity of fatty acids to the freshwater green alga Selenastrum capricornutum . Environmental Toxicology 18:5, pages 289-294.
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Maria S. Sepúlveda, Brian P. Quinn, Nancy D. Denslow, Stewart E. Holm & Timothy S. Gross. (2009) Effects of pulp and paper mill effluents on reproductive success of largemouth bass. Environmental Toxicology and Chemistry 22:1, pages 205-213.
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Li-Qun Wu, Heather D. Embree, Brian M. Balgley, Paul J. Smith & Gregory F. Payne. (2002) Utilizing Renewable Resources To Create Functional Polymers:  Chitosan-Based Associative Thickener. Environmental Science & Technology 36:15, pages 3446-3454.
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L. Mark Hewitt, Shirley Anne M. Smyth, Monique G. Dubé, Christine I. Gilman & Deborah L. MacLatchy. (2002) Isolation of compounds from bleached kraft mill recovery condensates associated with reduced levels of testosterone in mummichog ( Fundulus heteroclitus ) . Environmental Toxicology and Chemistry 21:7, pages 1359-1367.
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Marı́a S. Sepúlveda, William E. Johnson, John C. Higman, Nancy D. Denslow, Trenton R. Schoeb & Timothy S. Gross. (2002) An evaluation of biomarkers of reproductive function and potential contaminant effects in Florida largemouth bass (Micropterus salmoides floridanus) sampled from the St. Johns River. Science of The Total Environment 289:1-3, pages 133-144.
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Hiroshi Ishibashi, Makito Kobayashi, Tomohiko KoshiishiToshihisa MoriwakiKatsuyasu Tachibana, Mutsuyosi Tsuchimoto, Kiyoshi Soyano, Taisen Iguchi, Chisato Mori & Koji Arizono. (2002) Induction of Plasma Vitellogenin Synthesis by the Commercial Fish Diets in Male Goldfish(Carassius auratus) and Dietary Phytoestrogens.. Journal of Health Science 48:5, pages 427-434.
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Anna Tchoudakova, Mitsuyo Kishida, Elizabeth Wood & Gloria V Callard. (2001) Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. The Journal of Steroid Biochemistry and Molecular Biology 78:5, pages 427-439.
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Lynn P. Weber & David M. Janz. (2001) Effect of β-naphthoflavone and dimethylbenz[a]anthracene on apoptosis and HSP70 expression in juvenile channel catfish (Ictalurus punctatus) ovary. Aquatic Toxicology 54:1-2, pages 39-50.
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Mark E. McMaster, Janet J. Jardine, Gerald T. Ankley, William H. Benson, Mark S. GreeleyJr.Jr., Timothy S. Gross, Louis J. GuilletteJr.Jr., Deborah L. MacLatchy, Edward F. Orlando, Glen J. Van Der Kraak & Kelly R. Munkittrick. (2009) An interlaboratory study on the use of steroid hormones in examining endocrine disruption. Environmental Toxicology and Chemistry 20:9, pages 2081-2087.
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Erik Noaksson, Ulla Tjärnlund, Albertus T.C. Bosveld & Lennart Balk. (2001) Evidence for Endocrine Disruption in Perch (Perca fluviatilis) and Roach (Rutilus rutilus) in a Remote Swedish Lake in the Vicinity of a Public Refuse Dump. Toxicology and Applied Pharmacology 174:2, pages 160-176.
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Ronald Jenkins, Robert A. Angus, Heather McNatt, W. Mike Howell, Jon A. Kemppainen, Marion Kirk & Elizabeth M. Wilson. (2010) Identification of androstenedione in a river containing paper mill effluent. Environmental Toxicology and Chemistry 20:6, pages 1325-1331.
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K E Wynne-Edwards. (2001) Evolutionary biology of plant defenses against herbivory and their predictive implications for endocrine disruptor susceptibility in vertebrates.. Environmental Health Perspectives 109:5, pages 443-448.
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Monique G. Dubé & Deborah L. MacLatchy. (2001) Identification and treatment of a waste stream at a bleached-kraft pulp mill that depresses a sex steroid in the mummichog ( Fundulus heteroclitus ) . Environmental Toxicology and Chemistry 20:5, pages 985-995.
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David M Janz, Mark E McMaster, Lynn P Weber, Kelly R Munkittrick & Glen Van Der Kraak. (2001) Recovery of ovary size, follicle cell apoptosis, and HSP70 expression in fish exposed to bleached pulp mill effluent. Canadian Journal of Fisheries and Aquatic Sciences 58:3, pages 620-625.
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José Marı́a Navas & Helmut Segner. (2000) Antiestrogenicity of β-naphthoflavone and PAHs in cultured rainbow trout hepatocytes: evidence for a role of the arylhydrocarbon receptor. Aquatic Toxicology 51:1, pages 79-92.
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L. Mark Hewitt, Joanne L. Parrott, Kelly L. Wells, M. Kathryn Calp, Susan Biddiscombe, Mark E. McMaster, Kelly R. Munkittrick & Glen J. Van Der Kraak. (2000) Characteristics of Ligands for the Ah Receptor and Sex Steroid Receptors in Hepatic Tissues of Fish Exposed to Bleached Kraft Mill Effluent. Environmental Science & Technology 34:20, pages 4327-4334.
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