Skip to main content
SpringerLink
Log in

Hematological changes in yellowfin seabream (Acanthopagrus latus) following chronic exposure to bisphenol A

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

Bisphenol A (BPA) is one of the industrial chemical compounds which is produced in large volume throughout the world. It is a monomeric compound that is used in the manufacture of polycarbonate plastics and epoxy resins. The widespread use of BPA and its entry to aquatic ecosystems are serious problems. The aim of this study is to assess the change in the hematological parameters of Acanthopagrus latus as biomarkers after exposure to BPA in low concentrations at 1, 5, 10, and 50 (μg/g BPA). The experimental period was 21 days, and the injections were conducted in 0, 7, and 14 days in complete dose form. The blood collection from fishes was carried out in 14 and 21 days. Hematological profile, including red blood cells (RBCs), hematocrit (Ht), hemoglobin (Hb), MCH, MCV, MCHC, and white blood cell differential counts (lymphocytes, monocytes, basophils, eosinophils, and neutrophils) was conducted. The results of this study indicated that BPA has an inverse correlation with fish hematological parameter abnormalities; increasing concentration of BPA leads to a decrease in the RBC, Ht, Hb, secondary indices, and lymphocytes. Therefore, it was concluded that all the studied hematological parameters can be used as biomarkers for the presence of xenobiotic such as BPA in the natural environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. Available from http://www.statisticshowto.com/tables/f-table/.

References

  • Abalaka SE (2013) Evaluation of the haematology and biochemistry of Clarias gariepinus as biomarkers of environmental pollution in Tiga dam, Nigeria. Braz Arch Biol Technol 56:371–376. doi:10.1590/S1516-89132013000300004

    Article  CAS  Google Scholar 

  • Abou Khalil N, Abd-Elkareem M, Sayed A (2017) Nigella sativa seed protects against 4-nonylphenol-induced haematotoxicity in Clarias gariepinus (Burchell, 1822): oxidant/antioxidant rebalance. Aquac Nutr. doi:10.1111/anu.12522

  • Adedeji O, Adeyemo O, Agbede S (2009) Effects of diazinon on blood parameters in the African catfish (Clarias gariepinus). Afr J Biotechnol 8:3940

    CAS  Google Scholar 

  • Adhikari S, Sarkar B, Chatterjee A et al (2004) Effects of cypermethrin and carbofuran on certain hematological parameters and prediction of their recovery in a freshwater teleost, Labeo rohita (Hamilton). Ecotoxicol Environ Saf 58:220–226. doi:10.1016/j.ecoenv.2003.12.003

    Article  CAS  PubMed  Google Scholar 

  • Aghajanpour-Mir SM, Zabihi E, Akhavan-Niaki H et al (2016) The genotoxic and cytotoxic effects of bisphenol-a (BPA) in MCF-7 cell line and amniocytes. Int J Mol Cell Med 5:19

    PubMed  PubMed Central  Google Scholar 

  • Ahmed W, Moselhy W, Nabil T (2015) Bisphenol A toxicity in adult male rats: hematological, biochemical and histopathological approach. Glob Veternaria 14:228–238

    Google Scholar 

  • Babadi S, Safahiye A, Nabavi SMB, et al. (2014) The distribution mode of mercury in the different Acanthopagrus latus tissues, Moses estuary, Persian Gulf. Fisheries publication, Natural resources of Iran 68

  • Babu S, Uppu S, Claville MO et al (2013) Prooxidant actions of bisphenol A (BPA) phenoxyl radicals: implications to BPA-related oxidative stress and toxicity. Toxicol Mech Methods 23:273–280. doi:10.3109/15376516.2012.753969

    Article  CAS  PubMed  Google Scholar 

  • Bakker J, te Biesenbeek J, Boon P, et al. (2014) Bisphenol A: part 1. Facts and figures on human and environmental health issues and regulatory perspectives. RIVM rapport 601351001

  • Belfroid A, van Velzen M, van der Horst B et al (2002) Occurrence of bisphenol A in surface water and uptake in fish: evaluation of field measurements. Chemosphere 49:97–103. doi:10.1016/S0045-6535(02)00157-1

    Article  CAS  PubMed  Google Scholar 

  • Bhagwant S, Bhikajee M (2000) Induction of hypochromic macrocytic anaemia in Oreochromis hybrid (cichlidae) exposed to 100mg/l (sublethal dose) of aluminium. Univ Mauritius Res J 5:9–20

    Google Scholar 

  • Bhandari RK, Deem SL, Holliday DK et al (2015) Effects of the environmental estrogenic contaminants bisphenol A and 17α-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species. Gen Comp Endocrinol 214:195–219. doi:10.1016/j.ygcen.2014.09.014

    Article  CAS  PubMed  Google Scholar 

  • Bindhumol V, Chitra K, Mathur P (2003) Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 188:117–124. doi:10.1016/S0300-483X(03)00056-8

    Article  CAS  PubMed  Google Scholar 

  • Borst O, Abed M, Alesutan I et al (2012) Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Phys Cell Phys 302:C644–C651. doi:10.1152/ajpcell.00340.2011

    Article  CAS  Google Scholar 

  • Canesi L, Fabbri E (2015) Environmental effects of BPA focus on aquatic species. Dose-Response 13:1559325815598304. doi:10.1177/1559325815598304

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlisle J, Chan D, Golub M, et al. (2009) Toxicological profile for bisphenol A. D. Seigel (ed.), Office of Environmental Health Hazard Assessment. Prepared for Ocean Protection Council

  • Chitra K, Latchoumycandane C, Mathur P (2003) Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology 185:119–127. doi:10.1016/S0300-483X(02)00597-8

    Article  CAS  PubMed  Google Scholar 

  • Cossins AR, Crawford DL (2005) Fish as models for environmental genomics. Nat Rev Genet 6:324–333. doi:10.1038/nrg1590

    Article  CAS  PubMed  Google Scholar 

  • Cypher AD, Ickes JR, Bagatto B (2015) Bisphenol A alters the cardiovascular response to hypoxia in Danio rerio embryos. Comp Biochem Physio C Toxicol Pharmacol 174:39–45. doi:10.1016/j.cbpc.2015.06.006

    Article  Google Scholar 

  • de Carvalho PSM (2013) Behavioral biomarkers and pollution risks to fish health and biodiversity. In: Pollution and Fish Health in Tropical Ecosystems. CRC Press, pp 350–377

  • Desai B, Parikh P (2012) Impact of curzate (fungicide) on hematological parameters of Oreochromis mossambicus. Internat J Sci Engineer Res 3:1–6

    Google Scholar 

  • Fazio F, Faggio C, Marafioti S et al (2013) Effect of water quality on hematological and biochemical parameters of Gobius niger caught in Faro lake (Sicily). Iran J Fish Sci 12:219–231

    Google Scholar 

  • Flint S, Markle T, Thompson S et al (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manag 104:19–34. doi:10.1016/j.jenvman.2012.03.021

    Article  CAS  Google Scholar 

  • Gernhöfer M, Pawert M, Schramm M et al (2001) Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams. J Aquat Ecosyst Stress Recover 8:241–260. doi:10.1023/A:1012958804442

    Article  Google Scholar 

  • Hedayati A, Khsoravi Katuli K (2016) Impact of mercury on liver and ovary of yellowfin sea bream (Acanthopagrus latus) in the Persian Gulf. ECOPERSIA 4:1295–1312

    Article  Google Scholar 

  • Hedayati A, Safahieh A, Savar A et al (2010) Assessment of aminotransferase enzymes in yellowfin sea bream (Acanthopagrus latus) under experimental condition as biomarkers of mercury pollution. World J Fish Mar Sci 2:186–192

    CAS  Google Scholar 

  • Hesp SA, Potter IC, Hall NG (2004) Reproductive biology and protandrous hermaphroditism in Acanthopagrus latus. Environ Biol Fish 70:257–272. doi:10.1023/B:EBFI.0000033344.21383.00

    Article  Google Scholar 

  • Houston A (1990) Blood and circulation. Methods for fish biology 1990:273–334

    Google Scholar 

  • Howdeshell KL, Hotchkiss AK, Thayer KA et al (1999) Environmental toxins: exposure to bisphenol A advances puberty. Nature 401:763–764. doi:10.1038/44517

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim HA, Fouda MI, Yahya RS et al (2014) Erythrocyte phosphatidylserine exposure in β-thalassemia. Lab Hematol 20:9–14. doi:10.1532/LH96.12016

    Article  PubMed  Google Scholar 

  • Kavitha C, Malarvizhi A, Kumaran SS et al (2010) Toxicological effects of arsenate exposure on hematological, biochemical and liver transaminases activity in an Indian major carp, Catla catla. Food Chem Toxicol 48:2848–2854. doi:10.1016/j.fct.2010.07.017

    Article  CAS  PubMed  Google Scholar 

  • Keum Y-H, Jee J-H, Lee O-H et al (2005) In vivo effects of bisphenol A exposure on haematological parameters in Korean rockfish, Sebastes schlegeli. J Fish Pathol 18:293–300

    Google Scholar 

  • Khoshbavar-Rostami H, Soltani M, Hassan H (2006) Immune response of great sturgeon (Huso huso) subjected to long-term exposure to sublethal concentration of the organophosphate, diazinon. Aquaculture 256:88–94. doi:10.1016/j.aquaculture.2006.02.041

    Article  CAS  Google Scholar 

  • Kulkeaw K, Sugiyama D (2012) Zebrafish erythropoiesis and the utility of fish as models of anemia. Stem Cell Res Ther 3:55. doi:10.1186/scrt146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang E, Lang F (2015) Mechanisms and pathophysiological significance of eryptosis, the suicidal erythrocyte death. Semin cell Dev Biol:35–42. doi:10.1016/j.semcdb.2015.01.009

  • Lang IA, Galloway TS, Scarlett A et al (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300:1303–1310. doi:10.1001/jama.300.11.1303

    Article  CAS  PubMed  Google Scholar 

  • Maćczak A, Cyrkler M, Bukowska B et al (2016) Eryptosis-inducing activity of bisphenol A and its analogs in human red blood cells (in vitro study). J Hazard Mater 307:328–335. doi:10.1016/j.jhazmat.2015.12.057

    Article  PubMed  Google Scholar 

  • Madhu S and Pooja C. (2015) Acute toxicity of 4-nonylphenRes J Recent Sciol on haemotological profile of fresh water fish Channa punctatus. 2277: 2502

  • Meeker JD, Calafat AM, Hauser R (2010) Urinary bisphenol A concentrations in relation to serum thyroid and reproductive hormone levels in men from an infertility clinic. Environ Sci Technol 44:1458. doi:10.1021/es9028292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mekkawy IA, Mahmoud UM, Sayed AE-DH (2011) Effects of 4-nonylphenol on blood cells of the African catfish Clarias gariepinus (Burchell, 1822). Tissue Cell 43:223–229. doi:10.1016/j.tice.2011.03.006

    Article  CAS  PubMed  Google Scholar 

  • Melzer D, Rice NE, Lewis C et al (2010) Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One 5:e8673. doi:10.1371/journal.pone.0008673

    Article  PubMed  PubMed Central  Google Scholar 

  • Milla S, Depiereux S, Kestemont P (2011) The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review. Ecotoxicology 20:305–319. doi:10.1007/s10646-010-0588-7

    Article  CAS  PubMed  Google Scholar 

  • Narra MR (2017) Haematological and immune upshots in Clarias batrachus exposed to dimethoate and defying response of dietary ascorbic acid. Chemosphere 168:988–995. doi:10.1016/j.chemosphere.2016.10.112

    Article  CAS  PubMed  Google Scholar 

  • Nunes B, Gaio A, Carvalho F et al (2008) Behaviour and biomarkers of oxidative stress in Gambusia holbrooki after acute exposure to widely used pharmaceuticals and a detergent. Ecotoxicol Environ Saf 71:341–354. doi:10.1016/j.ecoenv.2007.12.006

    Article  CAS  PubMed  Google Scholar 

  • Onyia L, Michael K, Ekoto B (2013) Haematological profile, blood group and genotype of Heterobranchus bidorsalis. Net J Agric Sci 1:69–72

    Google Scholar 

  • Pait AS, Nelson JO (2003) Vitellogenesis in male Fundulusheteroclitus (killifish) induced by selected estrogenic compounds. Aquat Toxicol 64:331–342. doi:10.1016/S0166-445X(03)00060-2

    Article  CAS  PubMed  Google Scholar 

  • Peters G and Schwarzer R. (1985) Changes in hemopoietic tissue of rainbow trout under influence of stress. Diseases of aquatic organisms

  • Phuong LM, Damsgaard C, Ishimatsu A et al (2017) Recovery of blood gases and haematological parameters upon anaesthesia with benzocaine, MS-222 or Aqui-S in the air-breathing catfish Pangasianodon hypophthalmus. Ichthyol Res 64:84–92. doi:10.1007/s10228-016-0545-4

    Article  Google Scholar 

  • Qiu W, Chen J, Li Y et al (2016) Oxidative stress and immune disturbance after long-term exposure to bisphenol A in juvenile common carp (Cyprinus carpio). Ecotoxicol Environ Saf 130:93–102. doi:10.1016/j.ecoenv.2016.04.014

    Article  CAS  PubMed  Google Scholar 

  • Rao JV (2006) Biochemical alterations in euryhaline fish, Oreochromis mossambicus exposed to sub-lethal concentrations of an organophosphorus insecticide, monocrotophos. Chemosphere 65:1814–1820. doi:10.1016/j.chemosphere.2006.04.015

    Article  CAS  PubMed  Google Scholar 

  • Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77:229–238. doi:10.1016/j.aquatox.2005.10.018

    Article  CAS  PubMed  Google Scholar 

  • Roberts R (2001) The anatomy and physiology of teleosts. Fish Pathol:12–54

  • Rogers JA, Mirza RS (2013) The effects of bisphenol-A on the immune system of wild yellow perch, Perca flavescens. Water Air Soil Pollut 224:1728. doi:10.1007/s11270-013-1728-5

    Article  Google Scholar 

  • Savill J, Wyllie A, Henson J et al (1989) Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 83:865. doi:10.1172/JCI113970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sowemimo-Coker SO (2002) Red blood cell hemolysis during processing. Transfus Med Rev 16:46–60. doi:10.1053/tmrv.2002.29404

    Article  PubMed  Google Scholar 

  • Svoboda M, Luskova V, Drastichova J et al (2001) The effect of diazinon on haematological indices of common carp (Cyprinus carpio L.) Acta Vet Brno 70:457–465

    Article  CAS  Google Scholar 

  • Thien K. (2009) Bis-phenol A: origin, fate, dilemma and the effects of increased background organics on its adsorption by powdered activated carbon. TAMK University of Applied Sciences. 41p

  • Ulutaş OK, Yıldız N, Durmaz E et al (2011) An in vivo assessment of the genotoxic potential of bisphenol A and 4-tert-octylphenol in rats. Arch Toxicol 85:995–1001. doi:10.1007/s00204-010-0620-y

    Article  PubMed  Google Scholar 

  • Uribe C, Folch H, Enriquez R et al (2011) Innate and adaptive immunity in teleost fish: a review. Veterinarni Medicina 56:486–503

    CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. doi:10.1016/S1382-6689(02)00126-6

    Article  PubMed  Google Scholar 

  • Van Vuren J (1986) The effects of toxicants on the haematology of Labeo umbratus (Teleostei: Cyprinidae). Comp Biochem Physiol Part C Compar Pharmacol 83:155–159. doi:10.1016/0742-8413(86)90029-0

    Article  Google Scholar 

  • Vandenberg LN, Ehrlich S, Belcher SM et al (2013) Low dose effects of bisphenol A: an integrated review of in vitro, laboratory animal, and epidemiology studies. Endocrine disruptors 1:e26490. doi:10.4161/endo.26490

    Article  Google Scholar 

  • Vázquez GR, Nostro FL (2014) Changes in hematological parameters of Cichlasoma dimerus (Teleostei, Perciformes) exposed to sublethal concentrations of 4-tert-octylphenol. Arch Environ Contam Toxicol 66:463–469. doi:10.1007/s00244-014-9997-6

    Article  Google Scholar 

  • Verde, C., D. Giordano & G. di Prisco, 2011b. Erythropoiesis in fishes. In Farrell, T. (ed.), On-Line Encyclopaedia of Fish Physiology, from Genome to Environment, Vol. 2. Academic Press, San Diego: 992–997. ​doi:10.1016/B978-0-12-374553-8.00268-9

  • Verslycke T, Vandenbergh GF, Versonnen B et al (2002) Induction of vitellogenesis in 17α-ethinylestradiol-exposed rainbow trout (Oncorhynchus mykiss): a method comparison. Comp Biochem Physiol Part C Toxicol Pharmacol 132:483–492. doi:10.1016/S1532-0456(02)00111-4

    Article  Google Scholar 

  • Wei X, Huang Y, Wong MH et al (2011) Assessment of risk to humans of bisphenol A in marine and freshwater fish from Pearl River Delta, China. Chemosphere 85:122–128. doi:10.1016/j.chemosphere.2011.05.038

    Article  CAS  PubMed  Google Scholar 

  • Wepener V, Vuren J, Preez H (1992) Effect of manganese and iron at a neutral and acidic pH on the hematology of the banded tilapia (Tilapia sparrmanii). Bull Environ Contam Toxicol 49:613–619. doi:10.1016/j.chemosphere.2011.05.038

    Article  CAS  PubMed  Google Scholar 

  • Wozniak M, Murias M (2008) Xenoestrogens: endocrine disrupting compounds. Ginekol Pol 79:785–790

    PubMed  Google Scholar 

  • Yang YJ, Hong Y-C, Oh S-Y et al (2009) Bisphenol A exposure is associated with oxidative stress and inflammation in postmenopausal women. Environ Res 109:797–801. doi:10.1016/j.envres.2009.04.014

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Cooke GM, Curran IH et al (2011) GC–MS analysis of bisphenol A in human placental and fetal liver samples. J Chromatogr B 879:209–214. doi:10.1016/j.jchromb.2010.11.031

    Article  CAS  Google Scholar 

  • Zhu P, Tang Y, Fan J et al (2017) Hematological parameters and blood cell morphology of male and female Schizothorax (Racoma) davidi (Sauvage). J World Aquacult Soc. doi:10.1111/jwas.12397

Download references

Author information

Authors and Affiliations

  1. Department of Marine Biology, Faculty of Marine Science, Khorramshahr University of Marine Science and Technology, Khorramshahr, Islamic Republic of Iran

    Zeinab Yaghoobi, Alireza Safahieh, Mohammad Taghi Ronagh & Abdulali Movahedinia

  2. Department of Fisheries, Faculty of Marine Natural Resources, Khorramshahr University of Marine Science and Technology, Khorramshahr, Islamic Republic of Iran

    Seyed Mohammad Mousavi

Authors
  1. Zeinab Yaghoobi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alireza Safahieh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammad Taghi Ronagh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdulali Movahedinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Seyed Mohammad Mousavi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alireza Safahieh.

Ethics declarations

Conflict of interest

Author Zeinab Yaghoobi declares that she has no conflict of interest.

Author Alireza Safahieh declares that he has no conflict of interest.

Author Mohammad Taghi Ronagh declares that he has no conflict of interest.

Author Abdulali Movahedinia declares that he has no conflict of interest.

Author Seyed Mohammad Mousavi declares that he has no conflict of interest.

Funding

This study was not funded by any grant.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yaghoobi, Z., Safahieh, A., Ronagh, M.T. et al. Hematological changes in yellowfin seabream (Acanthopagrus latus) following chronic exposure to bisphenol A. Comp Clin Pathol 26, 1305–1313 (2017). https://doi.org/10.1007/s00580-017-2530-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-017-2530-3

Keywords

Search

Navigation