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Chronic Exposure to Water of Lake Qaroun Induced Metal-Related Testicular Damage and Endocrine Disruption in Male Fish

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Abstract

The uncontrolled releasing of hazardous wastes into Lake Qaroun was adversely impacting the aquatic environment and its biota. Therefore, this approach was designed to investigate the impact of these discharges on the reproductive and testicular function of Oreochromis niloticus. Several biomarkers were applied on the testicular tissues as metal bioaccumulation levels, histological examination with recording the ovotestis appearance and antioxidant status after 45 days of exposure to 0, 10, 20, & 30% of Lake Qaroun water (LQW). The bioaccumulated Cu, Mn, Fe, Pb, and Cd were unequally distributed in the testes but all these metals showed a significant concentration-dependent elevation among the studied groups. The exposure to LQW significantly increased the histological alterations in the testicular tissues as vacuolar degeneration, loss of tubular organization, and degeneration of Leydig cell. Based on the frequent appearance of histopathological abnormalities and ovotestis recording, the most deformed testicular tissues were observed in the 30% LQW-exposed groups. The ovotestis severity index (OSI) was significantly raised in LQW-exposed groups compared to the control group. The activities of superoxide dismutase, catalase as well as glutathione-reduced levels were significantly (p < 0.05) decreased in testes after chronic exposure to LQW. On the other pole, the activities of glutathione peroxidase enzyme and malondialdehyde formation were sharply increased. In view of the above, the exposure to LQW induced metal-related oxidative damage to the testicular tissues and impaired the male reproductive health. This study showed strong correlations between the anthropogenic activities around Lake Qaroun and the reproductive dysfunction in fish.

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References

  1. Tatar SY, Obek E, Yildirim NC (2017) Antioxidant response in duckweed after exposure to secondary effluent from municipal wastewater treatment plant, Elazığ, Turkey. Bull Environ Contam Toxicol 99(3):399–404. https://doi.org/10.1007/s00128-017-2133-3

    Article  CAS  PubMed  Google Scholar 

  2. Mansour S, Sidky M (2003) Ecotoxicological studies. 6. The first comparative study between Lake Qarun and Wadi El-Rayan wetland, with respect to contamination of their major components. Food Chem 82(2):181–189. https://doi.org/10.1016/S0308-8146(02)00451-X

    Article  CAS  Google Scholar 

  3. Omar WA, Zaghloul KH, Abdel-Khalek AA, Abo-Hegab S (2012) Genotoxic effects of metal pollution in two fish species, Oreochromis niloticus and Mugil cephalus, from highly degraded aquatic habitats. Mutat Res 746(1):7–14. https://doi.org/10.1016/j.mrgentox.2012.01.013

    Article  CAS  PubMed  Google Scholar 

  4. Ali MH, Fishar MR (2005) Accumulation of trace metals in some benthic invertebrate and fish species relevant to their concentration in water and sediment of Lake Qarun. Egypt J Aquat Res 31:289–301

    CAS  Google Scholar 

  5. Omar WA, Zaghloul KH, Abdel-Khalek AA, Abo-Hegab S (2013) Risk assessment and toxic effects of metal pollution in two cultured and wild fish species from highly degraded aquatic habitats. Arch Environ Contam Toxicol 65(4):753–764. https://doi.org/10.1007/s00244-013-9935-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sabae SZ, Mohamed FAS (2015) Effect of environmental pollution on the health of tilapia spp. from lake Qarun. Glob Vet 14(3):304–328

    CAS  Google Scholar 

  7. Choe SY, Kim SJ, Kim HG, Lee JH, Choi Y, Lee H, Kim Y (2003) Evaluation of estrogenicity of major heavy metals. Sci Total Environ 312(1-3):15–21. https://doi.org/10.1016/S0048-9697(03)00190-6

    Article  CAS  PubMed  Google Scholar 

  8. Martin MB, Reiter R, Pham T, Avellanet YR, Camara J, Lahm M, Pentecost E, Pratap K, Gilmore BA, Divekar S, Dagata RS, Bull JL, Stoica A (2003) Estrogen-like activity of metals in MCF-7 breast cancer cells. Endocrinology 144(6):2425–2436. https://doi.org/10.1210/en.2002-221054

    Article  CAS  PubMed  Google Scholar 

  9. Esteban S, Moreno-Merino L, Matellanes R, Catalá M, Gorga M, Petrovic M, López de Alda M, Barceló D, Silva A, Durán JJ, López-Martínez J, Valcárcel Y (2016) Presence of endocrine disruptors in freshwater in the northern Antarctic Peninsula region. Environ Res 147:179–192. https://doi.org/10.1016/j.envres.2016.01.034

    Article  CAS  PubMed  Google Scholar 

  10. Goksøyr A (2006) Endocrine disruptors in the marine environment: mechanisms of toxicity and their influence on reproductive processes in fish. J Toxicol Environ Health Part A 69(1-2):175–184. https://doi.org/10.1080/15287390500259483

    Article  CAS  Google Scholar 

  11. Tyler CR, Jobling S (2008) Roach, sex, and gender-bending chemicals: the feminization of wild fish in English Rivers. Bioscience 58(11):1051–1059. https://doi.org/10.1641/B581108

    Article  Google Scholar 

  12. Abdel-Moneim A, Coulter DP, Mahapatra CT, Sepulveda MS (2015) Intersex in fishes and amphibians: population implications, prevalence, mechanisms and molecular biomarkers. J Appl Toxicol 35(11):1228–1240. https://doi.org/10.1002/jat.3204

    Article  CAS  PubMed  Google Scholar 

  13. Allen Y, Scott AP, Matthiessen P, Haworth S, Thain JE, Feist SW (1999) Survey of estrogenic activity in United Kingdom estuarine and coastal waters and its effect on gonadal development of the flounder Platicthys flesus. Environ Toxicol Chem 18(8):1791–1800. https://doi.org/10.1002/etc.5620180827

    Article  CAS  Google Scholar 

  14. Simpson MG, Parry M, Kleinkauf A, Swarbreck D, Walker P, Leah RT (2000) Pathology of the liver, kidney, and gonad of flounder (Platichthys flesus) from a UK estuary impacted by endocrine-disrupting chemicals. Mar Environ Res 50(1-5):283–287. https://doi.org/10.1016/S0141-1136(00)00089-1

    Article  CAS  PubMed  Google Scholar 

  15. Nolan M, Jobling S, Brighty G, Sumpter JP, Tyler CR (2001) A histological description of intersexuality in the roach. J Fish Biol 58(1):160–176. https://doi.org/10.1111/j.1095-8649.2001.tb00505.x

    Article  Google Scholar 

  16. Feist SW, Stentiford GD, Kent ML, Ribeiro Santos A, Lorance P (2015) Histopathological assessment of liver and gonad pathology in continental slope fish from the northeast Atlantic Ocean. Mar Environ Res 106:42–50. https://doi.org/10.1016/j.marenvres.2015.02.004

    Article  CAS  PubMed  Google Scholar 

  17. Sharma RK, Agarwal A (1996) Role of reactive oxygen species in male infertility. Urology 48(6):835–850. https://doi.org/10.1016/S0090-4295(96)00313-5

    Article  CAS  PubMed  Google Scholar 

  18. Adedara IA, Lawal TA, Adesina AA, Oyebiyi OO, Ebokaiwe AP, Farombi EO (2014) Sperm functional parameters and erythrocytes oxidant-antioxidant imbalance during municipal landfill leachate treatment withdrawal in rats. Environ Toxicol Pharmacol 37(1):460–467. https://doi.org/10.1016/j.etap.2014.01.002

    Article  CAS  PubMed  Google Scholar 

  19. Sanocka D, Kurpisz M (2004) Reactive oxygen species and sperm cells. Reprod Biol Endocrinol 2:1–7

    Article  Google Scholar 

  20. Henkel R (2005) The impact of oxidants on sperm functions. Andrologia 37(6):205–206. https://doi.org/10.1111/j.1439-0272.2005.00699.x

    Article  CAS  PubMed  Google Scholar 

  21. Oyagbemi AA, Adedara IA, Saba AB, Farombi EO (2010) Role of oxidative stress in reproductive toxicity induced by co-administration of chloramphenicol and multivitamin haematinics complex in rats. Basic Clin Pharmacol Toxicol 107(3):703–708. https://doi.org/10.1111/j.1742-7843.2010.00561.x

    Article  CAS  PubMed  Google Scholar 

  22. Marentette J, Corkum L (2008) Does the reproductive status of male round gobies (Neogobius melanostomus) influence their response to conspecific odours? Environ Biol Fish 81(4):447–455. https://doi.org/10.1007/s10641-007-9240-7

    Article  Google Scholar 

  23. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, New York

    Google Scholar 

  24. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22(1):25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x

    Article  Google Scholar 

  25. Bateman KS, Stentiford GD, Feist SW (2004) A ranking system for the evaluation of intersex condition in European Flounder (Platichthys flesus). Environ Toxicol Chem 23(12):2831–2836. https://doi.org/10.1897/03-541.1

    Article  PubMed  Google Scholar 

  26. Nishikimi M, Appaji N, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46(2):849–854. https://doi.org/10.1016/S0006-291X(72)80218-3

    Article  CAS  PubMed  Google Scholar 

  27. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3

    Article  CAS  PubMed  Google Scholar 

  28. Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  PubMed  Google Scholar 

  29. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358. https://doi.org/10.1016/0003-2697(79)90738-3

    Article  CAS  PubMed  Google Scholar 

  30. Adedara IA, Awogbindin IO, Adesina AA, Oyebiyi OO, Lawal TA, Farombi EO (2015) Municipal landfill leachate-induced testicular oxidative damage is associated with biometal accumulation and endocrine disruption in rats. Arch Environ Contam Toxicol 68(1):74–82. https://doi.org/10.1007/s00244-014-0075-x

    Article  CAS  PubMed  Google Scholar 

  31. Jobling S, Sheahan D, Osborn JA, Mathiessen P, Sumpter JP (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 15(2):194–202. https://doi.org/10.1002/etc.5620150218

    Article  CAS  Google Scholar 

  32. Kime DE (1999) A strategy for assessing the effects of xenobiotics on fish reproduction. Sci Total Environ 225(1–2):3–11. https://doi.org/10.1016/S0048-9697(98)00328-3

    Article  CAS  PubMed  Google Scholar 

  33. Billard R, Breton B, Richard M (1981) On the inhibitory effects of some steriods on spermatogenesis in adult rainbow trout (Salmo gairdneri). Can J Zool 59(8):1479–1487. https://doi.org/10.1139/z81-201

    Article  CAS  Google Scholar 

  34. Iavicoli I, Fontana L, Bergamaschi A (2009) The effects of metals as endocrine disruptors. J Toxicol Environ Health B Crit Rev 12(3):206–223. https://doi.org/10.1080/10937400902902062

    Article  CAS  PubMed  Google Scholar 

  35. Hontela A, Lacroix A (2006) Heavy metals. In: Norris D, Carr JA (eds) Endocrine disruption: biological bases for health effects in wildlife and humans. Oxford University Press, Nova York, pp 356–374

    Google Scholar 

  36. Matthiessen P, Johnson I (2007) Implications of research on endocrine disruption for the environmental risk assessment, regulation and monitoring of chemicals in the European Union. Environ Pollut 146(1):9–18. https://doi.org/10.1016/j.envpol.2006.05.036

    Article  CAS  PubMed  Google Scholar 

  37. Rodríguez EM, Medesani DA, Fingerman M (2007) Endocrine disruption in crustaceans due to pollutants: a review. Comp Biochem Physiol A 146(4):661–671. https://doi.org/10.1016/j.cbpa.2006.04.030

    Article  CAS  Google Scholar 

  38. Huang YL, Tseng WC, Lin TH (2001) In vitro effects of metal ions (Fe2+, Mn2+, Pb2+) on sperm motility and lipid peroxidation in human semen. J Toxicol Environ Health A 62(4):259–267. https://doi.org/10.1080/009841001459414

    Article  CAS  PubMed  Google Scholar 

  39. Ponnapakkam TP, Bailey KS, Graves KA, Iszard MB (2003) Assessment of male reproductive system in the CD-1 mice following oral manganese exposure. Reprod Toxicol 17(5):547–551. https://doi.org/10.1016/S0890-6238(03)00101-1

    Article  CAS  PubMed  Google Scholar 

  40. Ramamoorthi RV, Rossano MG, Paneth N, Gardiner JC, Diamond MP, Puscheck E, Daly DC, Potter RC, Wirth JJ (2008) An application of multivariate ranks to assess effects from combining factors: metal exposures and semen analysis outcomes. Stat Med 27(18):3503–3514. https://doi.org/10.1002/sim.3236

    Article  CAS  PubMed  Google Scholar 

  41. Aydemir B, Kiziler AR, Onaran I, Alici B, Ozkara H, Akyolcu MC (2006) Impact of Cu and Fe concentrations on oxidative damage in male infertility. Biol Trace Elem Res 112(3):193–203. https://doi.org/10.1385/BTER:112:3:193

    Article  CAS  PubMed  Google Scholar 

  42. Sainath SB, Meena R, Supriya C, Reddy KP, Reddy PS (2011) Protective role of Centella asiatica on lead-induced oxidative stress and suppressed reproductive health in male rats. Environ Toxicol Pharmacol 32(2):146–154. https://doi.org/10.1016/j.etap.2011.04.005

    Article  CAS  PubMed  Google Scholar 

  43. Lafuente A, Cano P, Esquifino AI (2003) Are cadmium effects on plasma gonadotropins, prolactin, ACTH, GH and TSH levels, dose-dependent? Biometals 16(2):243–250. https://doi.org/10.1023/A:1020658128413

    Article  CAS  PubMed  Google Scholar 

  44. Akinloye O, Arowojolu AO, Shittu OB, Anetor JI (2006) Cadmium toxicity: a possible cause of male infertility in Nigeria. Reprod Biol 6(1):17–30

    PubMed  Google Scholar 

  45. Siu ER, Mruk DD, Porto CS, Cheng CY (2009) Cadmium-induced testicular injury. Toxicol Appl Pharmacol 238(3):240–249. https://doi.org/10.1016/j.taap.2009.01.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Van Aerle R, Nolan TM, Jobling S, Christiansen LB, Sumpter JP, Tyler CR (2001) Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ Toxicol Chem 20(12):2841–2847. https://doi.org/10.1002/etc.5620201225

    Article  PubMed  Google Scholar 

  47. Stentiford GD, Feist SW (2005) First case of intersex (ovotestis) in the flatfish species, dab (Limanda limanda): Dogger Bank, North Sea. Mar Ecol Prog Ser 301:307–310. https://doi.org/10.3354/meps301307

    Article  Google Scholar 

  48. Dietrich DR, Krieger HO (2009) Histological analysis of endocrine disruptive effects in small laboratory fish. Dietrich DR, Krieger HO, editors New Jersey: Wiley

  49. Li N, Hou YH, Ma DD, Jing WX, Dahms HU, Wang L (2015) Lead accumulation, oxidative damage and histopathological alteration in testes and accessory glands of freshwater crab, Sinopotamon henanense, induced by acute lead exposure. Ecotoxicol Environ Saf 117:20–27. https://doi.org/10.1016/j.ecoenv.2015.03.019

    Article  CAS  PubMed  Google Scholar 

  50. Kumar TR, Doreswamy K, Shrilatha B, Muralidhara (2002) Oxidative stress associated DNA damage in testis of mice: induction of abnormal sperms and effects on fertility. Mutat Res 513:103–111, 1-2, DOI: https://doi.org/10.1016/S1383-5718(01)00300-X

    Article  CAS  Google Scholar 

  51. Adedara IA, Farombi EO (2010) Induction of oxidative damage in the testes and spermatozoa and hematotoxicity in rats exposed to multiple doses of ethylene glycol monoethyl ether. Hum Exp Toxicol 29(10):801–812. https://doi.org/10.1177/0960327109360115

    Article  CAS  PubMed  Google Scholar 

  52. Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13(12):3145–3175. https://doi.org/10.3390/ijms13033145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, Faculty of Science, Cairo University, Giza, Egypt

    Amr A. Abdel-Khalek

  2. Medical Science Department, Faculty of Dentistry, The British University in Egypt, Cairo, Egypt

    Amr A. Abdel-Khalek

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“All procedures performed in this study involving animals (fish) were in accordance with the ethical standards of Faculty of Science, Cairo University, Institutional Animal Care and Use Committee (IACUC) at which the studies were conducted.”

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Abdel-Khalek, A.A. Chronic Exposure to Water of Lake Qaroun Induced Metal-Related Testicular Damage and Endocrine Disruption in Male Fish. Biol Trace Elem Res 185, 197–204 (2018). https://doi.org/10.1007/s12011-017-1220-y

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