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Biomarker-assisted assessment of aquatic health using the cosmopolitan common carp, Cyprinus carpio (L): a case study of bisphenol-A exposures

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Abstract

Monitoring aquatic health from environmental pollutants is critical, none more so than bisphenol-A (BPA), a ubiquitous endocrine-disrupting chemical (EDC). The present study brings out the responses of selected transcripts, hormone levels, and tissue histomorphology in a widely distributed fish species Cyprinus carpio (Linn.), following exposure to environmentally relevant (10, 100 ng/L) and higher (1000 ng/L) concentration of BPA. The response of cyp19a1a, cyp19a1b, and c3 significantly decreased, while that of vtg increased in their respective tissue domains. The hematological parameters TEC, Hb, and Hct decreased significantly in contrast to TLC (p < 0.05) at all exposure concentrations, whereas none of the erythrocytic indices (MCV, MCH, and MCHC) was perturbed. The steroidogenic hormone levels, such as estradiol and progesterone, increased significantly with increasing BPA concentrations. In contrast, the testosterone and all the thyroid hormones (T3, T4, and TSH) were suppressed significantly (p < 0.05). At the histological level, the BPA induced chondrocyte proliferation, which was accompanied by hemorrhage of the gill lamellae, increased melanomacrophagic centers (MMCs), and degeneration of tubules and fluid accumulation in the kidney. In parallel, binucleated hepatocytes and inflammations were prominent in the liver. Collectively, the histomorphology confirmed induction of degenerative effects in all the tissues investigated, while the cyclic responses of biochemical markers suggest an ability to regulate the impacts. However, a chronic exposure could result in overriding the endemic reproductive pathways with potential population-level effects. In conclusion, the study identified multiple molecular, cellular, and physiological markers that could be employed to detect early signs of BPA and more broadly EDC exposures. These markers in combination with a wide distribution of C. carpio should allow comparative studies of pollutants at environmental concentrations.

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References

  • Ahmed MK, Habibullah-Al-Mamun M, Parvin E, Akter MS, Khan MS (2013) Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, tilapia (Oreochromis mossambicus). Exp Toxicol Pathol 65(6):903–909

    CAS  Google Scholar 

  • Aiswarya KS, James R (2016) Effect of bisphenol A on certain hematological parameters of Heteropneustes fossilis, Bloch. Int J Emerging Trends Sci Tech 3(8):4493–4497

    Google Scholar 

  • Akram R, Iqbal R, Hussain R, Jabeen F, Ali M (2021) Evaluation of oxidative stress, antioxidant enzymes and genotoxic potential of bisphenol A in fresh water bighead carp (Aristichthys nobils) fish at low concentrations. Environ Pollut. https://doi.org/10.1016/j.envpol.2020.115896

  • Altun S, Ozdemir S, Arslan H (2017) Histopathological effects, responses of oxidative stress, inflammation, apoptosis biomarkers and alteration of gene expressions related to apoptosis, oxidative stress, and reproductive system in chlorpyrifos-exposed common carp (Cyprinus carpio L.). Environ Pollut 230:432–443

    CAS  Google Scholar 

  • Aluru N, Leatherland JF, Vijayan MM (2010) Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout. PLoS One 5(5):e10741

    Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater. 21st Edition. American Public Health Association. Washington, D.C.

  • Barney ML, Patil JG, Gunasekera RM, Carter CG (2008) Distinct cytochrome P450 aromatase isoforms in the common carp (Cyprinus carpio): sexual dimorphism and onset of ontogenic expression. Gen Comp Endocrinol 156(3):499–508

    CAS  Google Scholar 

  • Berczi I (1997) Pituitary hormones and immune function. Acta Paediatr Suppl 423:70–75

    CAS  Google Scholar 

  • Boyd CE (1998) Water quality for pond aquaculture. Research and development series no.43. International center for aquaculture and aquatic environments, Alabama Agricultural Experiment Station, Auburn University, Alabama.

  • Canesi L, Fabbri E (2015) Environmental effects of BPA: focus on aquatic species. Dose-Response 13:1–14

    CAS  Google Scholar 

  • Casanova-Nakayama A, Wenger M, Burki R, Eppler E, Krasnov A, Segner H (2011) Endocrine disrupting compounds: can they target the immune system of fish? Mar Pollut Bull 63(5-12):412–416

    CAS  Google Scholar 

  • Castro R, Abos B, Pignatelli J, von Gersdorff JL, Gonzalez Granja A, Buchmann K, Tafalla C (2014) Early immune responses in rainbow trout liver upon viral hemorrhagic septicemia virus (VHSV) infection. PLoS One 9(10):e111084

    Google Scholar 

  • Cervantes-Camacho I, Guerrero-Estévez SM, López MF, Alarcón-Hernández E, López-López E (2020) Effects of bisphenol A on Foxl2 gene expression and DNA damage in adult viviparous fish Goodea atripinnis. J Toxicol Environ Health A 83(3):95–112

    CAS  Google Scholar 

  • Chan WK, Chan KM (2012) Disruption of the hypothalamic- pituitary-thyroid axis in zebrafish embryo-larvae following water-borne exposure to BDE-47, TBBPA and BPA. Aquat Toxicol 108:106–111

    CAS  Google Scholar 

  • Colborn T, Saal FSV, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101:378–384

    CAS  Google Scholar 

  • Cornwell ER, Bellmund CA, Groocock GH, Wong PT, Hambury KL, Getchell RG, Bowser PR (2013) Fin and gill biopsies are effective nonlethal samples for detection of Viral hemorrhagic septicemia virus genotype IVb. J Vet Diagn Investig 25(2):203–209

    Google Scholar 

  • Corrales J, Kristofco LA, Steele WB, Yates BS, Breed CS, Williams ES, Brooks BW (2015) Global assessment of bisphenol A in the environment: Review and analysis of its occurrence and bioaccumulation. Dose-Response 13(3):1559325815598308

    Google Scholar 

  • Crain DA, Eriksen M, Iguchi T, Jobling S, Laufer H, LeBlanc GA, Guillette LJ Jr (2007) An ecological assessment of bisphenol-A: evidence from comparative biology. Reprod Toxicol 24:225–239

    CAS  Google Scholar 

  • Diaz N, Piferrer F (2017) Estrogen exposure overrides the masculinizing effect of elevated temperature by a downregulation of the key genes implicated in sexual differentiation in a fish with mixed genetic and environmental sex determination. BMC Genomics 18:973

    Google Scholar 

  • Dong Z, Li X, Huang S, Zhang N, Guo Y, Wang Z (2020) Vitellogenins and choriogenins are biomarkers for monitoring Oryzias curvinotus juveniles exposed to 17 β–estradiol. Comp Biochem Physiol C 236:108800. https://doi.org/10.1016/j.cbpc.2020.108800

    Article  CAS  Google Scholar 

  • Eichmiller JJ, Bajer PG, Sorensen PW (2014) The relationship between the distribution of common carp and their environmental DNA in a small lake. PLoS One 9(11):e112611

    Google Scholar 

  • Erkekoglu P, Kocer-Gumusel B (2016) Environmental effects of endocrine-disrupting chemicals: a special focus on phthalates and bisphenol A. Environ Heal Risk - Hazar Factors to Living Sp. https://doi.org/10.5772/62455

  • Evans DH (1987) The fish gill: site of action and model for toxic effects of environmental pollutants. Environ Health Perspect 71:47–58

    CAS  Google Scholar 

  • Faheem M, Jahan N, Lone KP (2016) Histopathological effects of bisphenol –A on liver, kidneys and gills of Indian major carp, Catla catla (Hamilton, 1822). J Ani Plant Sci 26(2):514–522

    CAS  Google Scholar 

  • Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manag 104:19–34

    CAS  Google Scholar 

  • Folmar LC, Penslow ND, Rao V, Chow M, Crain PA, Enblom J, Marcino J, Guilette LJ Jr (1996) Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ Health Perspect 104:1096–1101

    CAS  Google Scholar 

  • Gernhofer M, Pawert M, Schramm M, Müller E, Triebskorn R (2001) Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams. J Aquat Ecosyst Stress Recover 8:241–260

    CAS  Google Scholar 

  • Ghelichpour M, Mirghaed AT, Hoseinifar SH, Khalili M, Yousefi M, Doan HV, Perez-Jimenez A (2019) Expression of immune, antioxidant and stress related genes in different organs of common carp exposed to indoxacarb. Aquat Toxicol 208:208–216

    CAS  Google Scholar 

  • Gutierrez JB, Teem JL (2006) A model describing the effect of sex-reversed YY fish in an established wild population: the use of a Trojan Y-Chromosome to cause extinction of an introduced exotic species. J Theor Biol 241(22):333–341

    CAS  Google Scholar 

  • Hall JM, Greco CW (2020) Perturbation of nuclear hormone receptors by endocrine disrupting chemicals: mechanisms and pathological consequences of exposure. Cells 9(1):13

    CAS  Google Scholar 

  • Han JM, Park HJ, Kim JH, Jeong DS, Kang JC (2019) Toxic effects of arsenic on growth, hematological parameters, and plasma components of starry flounder, Platichthys stellatus, at two water temperature conditions. Fish Aquat Sci 22(1):1–8

    Google Scholar 

  • Haney DC, Hursh DA, Mix MC, Winton JR (1992) Physiological and hematological changes in chum salmon artificially infected with erythrocytic necrosis virus. J Aquat Anim Health 4:48–57

    Google Scholar 

  • Hinton DE, Lauren DJ (1990) Integrative histopathological approaches to detecting effects of environmental stressors on fishes. Am Fish Soc Symp 8:51–66

    Google Scholar 

  • Hinton DE, Segner H, Braunbeck T (2001) Toxic responses of the liver. In: Schlek D, Benson WH (eds) Target organ toxicity in marine and freshwater teleosts. Taylor & Francis, Boca Raton, pp 224–268

    Google Scholar 

  • Hulak M, Gazo I, Shaliutina A, Linhartova P (2013) In vitro effects of bisphenol A on the quality parameters, oxidative stress, DNA integrity and adenosine triphosphate content in sterlet (Acipenser ruthenus) spermatozoa. Comp Biochem Physiol C 158:64–71

    CAS  Google Scholar 

  • Hutchinson TH, Ankley GT, Segner H, Tyler CR (2006) Screening and testing for endocrine disruption in fish-biomarkers as “signposts,” not “traffic lights,” in risk assessment. Environ Health Perspect 1:106-114

  • Jha DK, Mishra BB, Thakur KR, Kumar V, Verma P, Khan PK (2017) Toxicological effects of arsenic exposure on haematology of fresh water fish Channa punctatus. Der Pharma Chemica 9(16):1–5

    Google Scholar 

  • John J, Gjessing ET, Grande M, Salbu B (1987) Influence of aquatic humus and pH on the uptake and depuration of cadmium by the Atlantic salmon (Salmo salar L.). Sci Total Environ 62:253–265

    CAS  Google Scholar 

  • Jung KK, Kim SY, Kim TG, Kang JH, Kanf SY, Cho JY, Kim SH (2007) Differential regulation of thyroid hormone receptor-mediated function by endocrine disruptors. Arch Pharm Res 30:616–623

    CAS  Google Scholar 

  • Kazeto Y, Place AR, Trant JM (2004) Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat Toxicol 69(1):25–34

    CAS  Google Scholar 

  • Kime D, Nash J, Scott AP (1999) Vitellogenesis as a biomarker of reproductive disruption by xenobiotics. Aquacult 177:345–352

    CAS  Google Scholar 

  • Kong RYC, Giesy JP, Wu RSS, Chen EXH, Chiang MWL, Lim BB, Yuen BBH, Yip BWP, Mok HOL, Au DWT (2008) Development of a marine fish model for studying in vivo molecular responses in ecotoxicology. Aquat Toxicol 86:131–141

    CAS  Google Scholar 

  • Lalonde B, Garron C (2020) Spatial and temporal distribution of BPA in the Canadian freshwater environment. Arch Environ Contam Toxicol 78:568–578. https://doi.org/10.1007/s00244-020-00721-2

    Article  CAS  Google Scholar 

  • Laing LV, Viana J, Dempster EL, Trznadel M, Trunkfield LA, Uren Webster TM, van Aerle R, Paull GC, Wilson RJ, Mill J, Santos EM (2016) Bisphenol A causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio). Epigenetics 11(7):526–538

    CAS  Google Scholar 

  • Liu Y, Yuan C, Chen S, Zheng Y, Zhang Y, Gao J, Wang Z (2014) Global and cyp19a1a gene specific DNA methylation in gonads of adult rare minnow Gobiocypris rarus under bisphenol A exposure. Aquat Toxicol 156:10–16

    CAS  Google Scholar 

  • Ljubojevic D, Radosavljevic V, Puvaca N, Balos MZ, Dorpevic V, Jovanovic R, Cirkovic M (2015) Interactive effects of dietary protein level and oil source on proximate composition and fatty acid composition in common carp (Cyprinus carpio L.). J Food Compos Anal 37:44–50

    CAS  Google Scholar 

  • Ma J, Feng Y, Xie W, Yang L, Li X (2015) Immune response in common carp (Cyprinus carpio L.) following glyphosate-exposure. Toxicol Rev 34(4):184–189

    CAS  Google Scholar 

  • Mandich A, Bottero S, Benfenati E, Cevasco A, Erratico C, Maggioni S, Massari A, Pedemonte F, Vigano L (2007) In vivo exposure of carp to graded concentrations of bisphenol A. Gen Comp Endocrinol 153(1-3):15–24

    CAS  Google Scholar 

  • Manikandan SR, Sukumaran M, Sridharan G, Muthukumaravel K, Ramya P, Rajeshwari K (2013) Hematological studies on freshwater catfish Mystus vittatus exposed to sodium arsenate. Int J Pure Appl Zool 1(4):310–314

    Google Scholar 

  • Maradonna F, Carnevali O (2018) Lipid metabolism alteration by endocrine disruptors in animal models: an overview. Front Endocrinol 9:654

    Google Scholar 

  • Mary JA, Jose KD (2018) Haematological profile of Channa striatus exposed to sublethal concentrations of endocrine disruptor chemical Triclosan. Int J Sci Res Rev 7(3):847–858

    CAS  Google Scholar 

  • Meng X, Shen Y, Wang S, Xu X, Dang Y, Zhang M, Li L, Zhang J, Wang R, Li J (2019) Complement component 3 (C3): an important role in grass carp (Ctenopharyngodon idella) experimentally exposed to Aeromonas hydrophila. Fish Shellfish Immunol 88:189–197

    CAS  Google Scholar 

  • Mohamed AAR, El-Houseiny W, EL-Murr AE, Ebraheim LLM, Ahmed AI, El-Hakim YMA (2020) Effect of hexavalent chromium exposure on the liver and kidney tissues related to the expression of CYP450 and GST genes of Oreochromis niloticus fish: role of curcumin supplemented diet. Ecotoxicol Environ Saf 188:109890. https://doi.org/10.1016/j.ecoenv.2019.109890

    Article  CAS  Google Scholar 

  • Moreman J, Lee O, Trznadel M, David A, Kudoh T, Tyler CR (2017) Acute toxicity, teratogenic, and estrogenic effects of bisphenol A and its alternative replacements bisphenol S, bisphenol F, and bisphenol AF in zebrafish embryo-larvae. Environ Sci Technol 51:12796–12805

    CAS  Google Scholar 

  • Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, Kanamoto N, Hataya Y, Shimatsu A, Kuzuya H, Nakao K (2002) Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 87(11):5185–5190

    CAS  Google Scholar 

  • Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32:1372–1379

    CAS  Google Scholar 

  • Naveenkumar BT, Kaur Y, Tyagi A, Shanthanagouda AH (2017) Baseline studies on selected hematological parameters of Indian major carps, exotic carps and catfishes. J Fish Life Sci 2:60–67

    Google Scholar 

  • Naz S, Hussain R, Ullah Q, Chatha AMM, Shaheen A, Khan RU (2020) Toxic effect of some heavy metals on hematology and histopathology of major carp (Catla catla). Environ Sci Pollut Res 28:6533–6539. https://doi.org/10.1007/s11356-020-10980-0

    Article  CAS  Google Scholar 

  • Nowak BF, Lucas CT (1997) Diagnosis of structural changes in fish gills-can biopsy replace necropsy? Aquaculture 159:1–10

    Google Scholar 

  • Nugegoda D, Kibria G (2016) Effects of environmental chemicals on fish thyroid function: Implications for fisheries and aquaculture in Australia. Gen Comp Endocrinol 244:40–53

    Google Scholar 

  • Patil JG, Gunasekera RM (2008) Tissue and sexually dimorphic expression of ovarian and brain aromatase mRNA in the Japanese medaka (Oryzias latipes): implications for their preferential roles in ovarian and neural differentiation and development. Gen Comp Endocrinol 158:131–137

    CAS  Google Scholar 

  • Piferrer F, Blazquez M (2005) Aromatase distribution and regulation in fish. Fish Physiol Biochem 31(2-3):215–226

    CAS  Google Scholar 

  • Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Muller R, Llyod R (eds) sublethal and chronic effects of pollution on freshwater fish. FAO, Fishing News Books, Oxford, pp 339–352

    Google Scholar 

  • Qiu W, Shen Y, Pan C, Liu S, Wu M, Yang M, Wang K (2016) The potential immune modulatory effect of chronic bisphenol A exposure on gene regulation in male medaka (Oryzias latipes) liver. Ecotoxicol Environ Saf 130:146–154

    CAS  Google Scholar 

  • Ramakrishnan S, Wayne NL (2008) Impact of bisphenol-A on early embryonic development and reproductive maturation. Reprod Toxicol 25:177–183

    CAS  Google Scholar 

  • Rashid M, Jabeen G, Nosheen S (2018) An exposure study of endocrine disruptors on haematology of fresh water fish Labeo rohita. Int J Biosci 12(2):137–141

    CAS  Google Scholar 

  • Sahli T (1962) Text book of clinical pathology. (Ed: Scward, Eimiller). Williams and Willams and Co., Baltimore. 35pp.

  • Sanchez W, Goin C, Brion F, Olsson PE, Goksøyr A, Porcher JM (2008) A new ELISA for the three-spined stickleback (Gasterosteus aculeatus L.) spiggin, using antibodies against synthetic peptide. Comp Biochem Physiol C 147:129–137

    CAS  Google Scholar 

  • Schwartz DA (2005) National Toxicology Program (NTP); Center for the evaluation of risks to human reproduction (CERHR); plans for future expert panel evaluation of Bisphenol A and hydroxyurea; requests for comments and nominations of scientists qualified to serve on these expert panels. Fed Regist 70:75827–75828

    Google Scholar 

  • Seemann F, Peterson DR, Witten PE, Guo BS, Shanthanagouda AH, Ye RR, Zhang G, Doris WTA (2015) Insight into the transgenerational effect of benzo[a]pyrene on bone formation in a teleost fish (Oryzias latipes). Comp Biochem Physiol C178:60–67

    Google Scholar 

  • Selvaraj KK, Shanmugam G, Sampath S, Larsson DG, Ramaswamy BR (2014) GC-MS determination of bisphenol A and alkylphenolethoxylates in river water from India and their ecotoxicological risk assessment. Ecotoxicol Environ Saf 99:13–20

    CAS  Google Scholar 

  • Shanthanagouda AH, Guo BS, Ye RR, Chao L, Chiang MWL, Singaram G, Napo KM, Cheung NKM, Ge Zhang ADWT (2014a) Japanese medaka: a non-mammalian vertebrate model for studying sex and age-related bone metabolism in vivo. PLoS One 9:e88165

    Google Scholar 

  • Shanthanagouda AH, Nugegoda D, Patil JG (2014b) Effects of bisphenol A and fadrozole exposures on cyp19a1 expression in the murray rainbowfish, Melanotaenia fluviatilis. Arch Environ Contam Toxicol 67:270–280

    CAS  Google Scholar 

  • Shanthanagouda AH, Patil JG, Nugegoda D (2013) Effects of exposure to oestrogenic compounds on aromatase gene expression are gender dependent in the rainbowfish. Melanotaenia fluviatilis Comp Biochem Physiol C157:162–171

  • Sisodiya M, Khare M, Kanhere RR (2018) Hepatotoxic effects of Bisphenol A on H. fossilis. Trends in Fisheries research 7(3):2319–4758

    Google Scholar 

  • Skidmore JF, Tovell PWA (1972) Toxic effects of zinc sulphate on the gills of rainbow trout. Water Res 6:217–248

    CAS  Google Scholar 

  • Staples C, van der Hoeven N, Clark K, Mihaich E, Woelz J, Hentges S (2018) Distributions of concentrations of bisphenol A in North American and European surface waters and sediments determined from 19 years of monitoring data. Chemosphere 201:448–458

    CAS  Google Scholar 

  • Sumuduni BGD, Munasinghe DHN, Arulkanthan AA (2018) Chronological analysis of the damages caused by the metacercariae of Centrocestus formosanus in the gills of Cyprinus carpio and lesions caused by the adult flukes in Ardeola ralloides: An experimental study. Int J Vet Sci Med 6:165–171

    Google Scholar 

  • Talas ZS, Pinar Dundar S, Fuat Gulhan M, Orun I, Kakoolaki S (2012) Effects of propolis on some blood parameters and enzymes in carp exposed to arsenic. Iran J Fish Sci 11(2):405–414

    Google Scholar 

  • Tohme M, Prud’homme SM, Boulahtouf A, Samarut E, Brunet F, Bernard L, Bourguet W, Gibert Y, Balaguer P, Laudet V (2014) Estrogen-related receptor γ is an in vivo receptor of Bisphenol A. The F.A.S.E.B. J. 28(7):3124–3133

    CAS  Google Scholar 

  • Tyler CR, Filby AL, Aerle RV, Lange A, Ball J, Santos EM (2008) Fish toxicogenomics. Adv Exp Biol 2:75–132

    CAS  Google Scholar 

  • Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24(2):139–177

    CAS  Google Scholar 

  • Vasu G, Sujatha LB, Manju Baishini J (2019) Histological changes in tilapia exposed to bisphenol A (BPA) compound. IntJ Adv Sci Res Manag 4(4):267–282

    Google Scholar 

  • Virk P, Al-Sakran AAM, Elobeid MA (2014) Effect of bisphenol A on the levels of vitellogenin and metallothionein in adult male carp, Cyprinus carpio carpio Linnaeus, 1758. Trop J Pharm Res 13(7):1107–1112

    Google Scholar 

  • Vousta D, Hartmann P, Schaffiner C, Giger W (2006) Benzitriozoles, alkylphenols and bisphenol A in municipal wastewaters and in the Glatt River, Switzerland. Environ Sci Pollut Res Int 13:333–341

    Google Scholar 

  • Wang J, Liu X, Wang H, Wu T, Hu X, Qin F, Wang Z (2010) Expression of two cytochrome P450 aromatase genes is regulated by endocrine disrupting chemicals in rare minnow Gobiocypris rarus juveniles. Comp Biochem Physiol C 152:313–320

    Google Scholar 

  • Wang H, Wu T, Qin F, Wang L, Wang Z (2012) Molecular cloning of Foxl2 gene and the effects of endocrine-disrupting chemicals on its mRNA level in rare minnow, Gobiocypris rarus. Fish Physiol Biochem 38(3):653–664

    CAS  Google Scholar 

  • Warner KE, Jenkins JJ (2007) Effects of 17 alpha-ethynilestradiol and bisphenol A on vertebral development in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 26(4):732–737

    CAS  Google Scholar 

  • Wolf JC, Wheeler JR (2018) A critical review of histopathological findings associated with endocrine and non-endocrine hepatic toxicity in fish models. Aquat Toxicol 197:60–78

    CAS  Google Scholar 

  • Wu M, Xu H, Shen Y, Qiu W, Yang M (2011) Oxidative stress in zebrafish embryos induced by short-term exposure to bisphenol A, nonylphenol, and their mixture. Environ Toxicol Chem 30(10):2335–2341

    CAS  Google Scholar 

  • Xu H, Yang M, Qiu W, Pan C, Wu M (2013) The impact of endocrine-disrupting chemicals on oxidative stress and innate immune response in zebrafish embryos. Environ Toxicol Chem 32(8):1793–1799

    CAS  Google Scholar 

  • Zoeller RT, Bansal R, Parris C (2005) Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinol 146(2):607–612

    CAS  Google Scholar 

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Acknowledgements

The authors thank the Dean, College of Fisheries, Guru Angad Dev Veterinary and Animal Sciences University (GADVASU), Ludhiana, Punjab, India, for the facilities and for making the study possible. Authors extend their gratitude to the Head, Department of Veterinary Anatomy, College of Veterinary Sciences and Head, Department of Animal Biotechnology, College of Animal Biotechnology GADVASU, for providing microscopy and real-time PCR facilities. The authors thank anonymous reviewers for their constructive criticisms and editorial suggestions which has improved the manuscript and for its better presentation.

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S.A.H., A.K., and N.B. performed the work; S.A.H., M.D.A., and J.G.P.: conceptualization of the experiment and wrote the manuscript; S.A.H., N.B.T., V.I.K., and R.S.S. analyzed the data. All authors read and approved the manuscript.

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Correspondence to Shanthanagouda Admane Holeyappa or Meera D. Ansal.

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Holeyappa, S.A., Kaur, A., Bansal, N. et al. Biomarker-assisted assessment of aquatic health using the cosmopolitan common carp, Cyprinus carpio (L): a case study of bisphenol-A exposures. Environ Sci Pollut Res 29, 14206–14218 (2022). https://doi.org/10.1007/s11356-021-16778-y

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