Effects of different sub-lethal concentrations of silver nanoparticles on thyroid hormones, growth hormone, blood factors and liver enzymes of common carp (Cyprinus carpio)

Document Type : Research Paper


1 Assistant Professor in Department of Marine Biology, Faculty of Sciences, Lahijan Branch, Islamic Azad University, Lahijan, Iran

2 M.Sc. in Marine Biology, Department of Marine Biology, Faculty of Sciences, Lahijan Branch, Islamic Azad University, Lahijan, Iran


Fish is in the highest level of aquatic food chain and has the ability to biologically magnify heavy metals, even at low concentrations in the environment. Biochemical methods and measuring blood parameters are among the important biological indicators that are widely used in assessing the health status of fish. The aim of this study was to investigate the effects of silver nanoparticles on thyroid hormones, growth hormone, blood factors and liver enzymes of common carp (Cyprinus carpio). In this study, 150 fish with weight of 12-15g after obtaining acute toxicity (LC50 96h), randomly exposed to concentrations of 0 (control), 5, 10 and 15 µg/L of LC50 96h silver nanoparticles with three replications for 7 days. At the end of the experimental period, blood samples were withdrawn by puncturing the vein in the fish tail. The results of this study showed that silver nanoparticles led to a significant difference in the number of white blood cells, percentage of neutrophils, lymphocytes and eosinophils and also amount of ALT and AST in the treatments (P<0.05). Also silver nanoparticles have negative effects on blood and biochemical parameters of common carp.


بیتا س.، مصباح م. و اکبری پ. 1396. تاثیر غلظت‌های مختلف نانوذرات نقره بر فاکتورهای خونی و بیوشیمیایی سرم خون ماهی شیربت (Barbus grypus) پرورشی در استان خوزستان. مجله علمی تحقیقات دامپزشکی و فرآورده‌های بیولوژیک، 30(3): 180-170.
جهانبخشی ع.، هدایتی ع.ا. و قادری رمازی ف. 1393. سم‌شناسی آبزیان. دانشگاه علوم کشاورزی و منابع طبیعی گرگان، 212ص.
جوهری س.ع. و حسینی س. 1393. سمیت تغذیه‌ای کلوئید نانوذرات نقره در ماهی قزل‌آلای رنگین‌کمان (Oncorhynchus mykiss). مجله علمی شیلات ایران، 23(1): 31-23.
رزمآرا پ.، پیکان حیرتی ف. و درافشان س. 1393. اثر نانوذرات نقره بر برخی شاخص‌های خون‌شناسی گربه‌ماهی رنگین‌کمان (Pangasius hypophthalmus). مجله سلول و بافت، 5(2): 272-263.
رضایی زارچی س. 1390. اثر نانوذرات اکسید تیتانیوم روی میزان سلول‌های خونی و آنزیم‌های کبدی موجود در خون رت نژاد ویستار. مجله دانشگاه علوم پزشکی و خدمات بهداشتی درمانی شهید صدوقی یزد، 19(5): 626-618.
زمینی ع.ع. 1375. تعیین غلظت کشنده LC5096h فلزات سرب و کادمیم بر روی دو گونه از کپور ماهیان چینی (آمور و فیتوفاگ). پایان‌نامه کارشناسی ارشد، دانشگاه آزاد اسلامی. 56ص.
ستاری م. 1381. ماهی‌شناسی (1)، تشریح و فیزیولوژی. انتشارات نقش مهر. 659ص.
شریعتی ف. 1382. تعیین سمیت و LC50 فنل و 1- نفتول روی ماهیان انگشت‌قد سیم و سفید. مجله علمی شیلات ایران، 12(4): 68-57.
ضیایی‌نژاد س.، دلاوریان ر.،  خاکی ف. و جوهری س. 1397. تجمع بافتی کلوئید نانوذرات نقره در بافت‌های آبشش و عضله ساقه دمی در ماهی کپور معمولی (Cyprinus carpio). توسعه آبزی‌پروری، 12(4): 94-83.
علیشاهی م. و مصباح م. 1389. مقایسه سمیت نانوذرات نقره در ماهیان آمور (Ctenopharyngodon idella)، شیربت (Barbus grypus)، اسکار (Astronoru ocellatus)، سوروم (Cichlosoma severums). مجله بیولوژی دریا، 2(7):51-45.
فروهر م.، ایمانپور م.، شعبانی ع. و هدایتی ع.ا. 1400. بررسی پاسخ‌های کشندگی نانوذرات نقره بر ماهی قرمز (Carassius auratus gibelio). فصلنامه علوم و تکنولوژی محیط زیست، 23(5): 80-71.
ملاحی ه. 1397. مقاوم‌سازی ماهی کپور معمولی (Cyprinus carpio) در مواجهه با نانونقره با استفاده از پروبیوتیک، پریبیوتیک و سین بیوتیک جیره. پایان‌نامه کارشناسی ارشد، دانشگاه علوم کشاورزی و منابع طبیعی گرگان. 79ص.
هدایتی ع.ا.، قربانی ر.، باقری ط.، احمدوند ش. و جهانبخشی ع. 1392. بررسی اثرات سمیت کشنده نانواکسید روی (Zno Nps)، نانواکسید مس (Cuo Nps) و نانودی‌اکسید تیتانیوم (Tio2 Nps) و بررسی اثرات سمیت تحت کشنده آن‌ها بر فاکتورهای خون و بافت آبشش ماهی قرمز، کپور معمولی و کلمه. طرح پژوهشی دانشگاه علوم کشاورزی و منابع طبیعی گرگان. 29ص.
Abdollahpour H., Falahatkar B., Efatpanah I., Meknatkhah B. annd Van Der Kraak G. 2018. Influence of thyroxine on spawning performance and larval development of Sterlet sturgeon Acipenser ruthenus. Aquaculture, 497: 134–139.
Acerete L., Balasch J.C., Espinosa E., Josa A. and Tort L. 2004. Physiological responses in Eurasian perch (Perca fluviatilis, L.) subjected to stress by transport and handling. Aquaculture, 237: 167–178.
Adams S.M. 2002. Biological Indicators of Aquatic Ecosystem Stress. American Fisheries Society, USA. 219P.
Alishahi M., Mohammadi A., Mesbah M. and Razi Jalali M. 2016. Haemato-immunological responses to diazinon chronic toxicity in Barbus sharpeyi. Iranian Journal of Fisheries Sciences, 15: 870–885.
Besson M., Feeney W.E., Moniz I., Francois L., Brooker R.M., Holzer G., Metian M., Roux N., Laudet V. and Lecchini D. 2020. Anthropogenic stressors impact fish sensory development and survival via thyroid disruption. Nature Communications, 11: 1–10.
Bhagwant S. and Bhikagee M. 2000. Induction of hypochromic macrocytic anemia in Oreochromis hybrid (Cichlidae) exposed to 100mg/L (sub lethal dose) of Aluminum. University of Mauritius Research Journal, 5: 9–20.
Blanton M.L. and Specker J.L. 2007. The hypothalamic-pituitary thyroid (hpt) axis in fish and its role in fish development and reproduction. Critical Reviews in Toxicology, 37: 97–115.
Blaxhall P. and Daisley K.W. 1972. Rutine hematological methods for use with fish blood. Journal of Fish Biology, 5: 771–781.
Canosa L.F., Chang J.P. and Peter R.E. 2007. Neuroendocrine control of growth hormone in fish. Endocrinology, 151: 1–26.
Chen C., Gregory Y. and Wooster P.R. 2004. Bowser comparative blood chemistry and histopathology of tilapia infected with Vibrio vulnificus or Streptococcus iniae or exposed to carbon tetrachloride, gentamicin, or copper sulfate. Aquaculture, 239: 421–443.
Chopra I. 2007. The increasing use of silver-based products as antimicrobial agents: A useful development or a cause for concern. Journal of Antimicrobial Chemotherapy, 59: 587–590.
Ellis A.E. 1971. The leukocytes of fish: A review. Journal of Fish Biology, 11: 453–491.
Ferguson R.M.W., Merrifield D.L., Harper G.M., Rawling M.D., Mustafa S., Picchietti S., Blacazar J.L. and Davies S.J. 2010. The effect of Pediococcus acidilactici on the gut microbiota and immune status of on growing red tilapia (Oreochromis niloticus). Journal of Applied Microbiology, 109: 851–862.
Hagmar L., Persson-Moschos M., Åkesson B. and Schutz A. 1998. Plasma levels of selenium, selenoprotein P and glutathione peroxidase and their correlations to fish intake and serum levels of thyrotropin and thyroid hormones: A study on Latvian fish consumers. European Journal of Clinical Nutrition, 52: 796–800.
Huang L. and Specker J.L. 1994. Growth hormone-and prolactin-producing cells in the pituitary gland of striped bass (Morone saxatilis): Immunocytochemical characterization at different life stages. General and Comparative Endocrinology, 94: 225–236.
Johari S.A., Kalbassi M.R., Soltani M. and Yu I.J. 2013. Toxicity comparison of colloidal silver nanoparticles in various life stages of rainbow trout (Oncorhynchus mykiss). Iranian Journal of Fisheries Sciences, 12: 76–95.
Jones I., Kille P. and Sweeney G. 2001. Cadmium delays growth hormone expression during rainbow trout development. Journal of Fish Biology, 59: 1015–1022.
Kandel E.R., Schwartz J.H., Jessell T.M., Siegelbaum S.A. and Hudspeth A.J. 2012. Principles of Neural Science. McGraw-Hill, USA. 1760P.
Karen V., Vitorovic S., Tutundzic V. and Poleksic V. 1998. Functional enzymes activity and gill histology of carp after copper sulfate exposure and recovery. Ecotoxicology and Environmental Safety, 40: 49–55.
Khabbazi M., Harsij M., Hedayati S.A., Gholipoor H., Gerami M.H. and Ghafari Farsani H. 2015. Effect of CuO nanoparticles on some hematological indices of rainbow trout (Oncorhynchus mykiss) and their potential    toxicity. International Journal of Nanomedicine, 2: 67–73.
Lal B. and Singh A.K. 2005. Immunological and physiological validation of enzyme-linked immunosorbent assay for growth hormone of the Asian catfish, Clarias batrachus. Fish Physiology and Biochemistry, 31: 289–293.
Lam S.H., Wu Y.L., Vega V.B., Miller L.D., Spitsbergen J., Tong Y., Zhan H., Lee S., Mathavan S., Murthy K.R.K., Buhler D.R., Liu E. and Gong Z. 2006. Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nature Biotechnology, 24: 73–75.
Leatherland J.F., Hilliard R.W., Macey D.J. and Potter I.C. 1990. Changes in serum thyroxine and triiodothyronine concentrations during metamorphosis of the Southern Hemisphere lamprey Geotria australis, and the effect of propylthiouracil, triiodothyronine and environmental temperature on serum thyroid hormone concentrations of ammocoetes. Fish Physiology and Biochemistry, 8: 167–177.
Lee J., Kim J., Shin Y., Ryu J.E. and Lee J.S. 2014. Serum and ultrastructure responses of common carp (Cyprinus carpio L.) during long-term exposure to and histopathology of the endangered Caspian brown trout (Salmo trutta caspius). Comparative Biochemistry and Physiology, 184: 28–35.
Louei Monfared A. and Soltani S. 2013. Effects of silver nanoparticles administration on the liver of rainbow trout (Oncorhynchus mykiss): histological and biochemical studies. European Journal of Experimental Biology, 3(2): 285–289.
Mortimer C.E. 1967. Chemistry: A Conceptual Approach.‏ Reinhold Publishing, USA. 692P.
Moss D.W. and Henderson A.R. 1999. Clinical enzymology. P: 617–721. In: Burtis C.A. and Ashwood E.R. (Eds.). Tietz Textbook of Clinical Chemistry. USA.
OECD (Organization Economic Cooperation Development). 2001. Guideline testing of chemicals: no.210. Section 2: Effect on biotic system divection. OECD, France. 139P.
Oner M., Atli G. and Canli M. 2009. Effects of metal (Ag, Cd, Cr, Cu, An) exposures on some enzymatic and non-enzymatic indicators in the liver of Oreochromis niloticus. Environmental Contamination and Toxicology, 82: 317–321.
Rad A., Alishahi M., Ghorbanpour M. and Zarei M. 2014. The effects of oral administration of extracted chitosan from white leg shrimp (Litopenaeus vannamei) on hematological and growth indices in common carp (Cyprinus carpio). Journal of Veterinary Research, 69: 385–393.
Ramsden S.R., Smith T.J., Shaw B.J. and Handy R.D. 2009. Dietary exposure to titanium dioxide nanoparticles in rainbow trout, (Oncorhynchus mykiss): No effect on growth, but subtle biochemical disturbances in the brain. Ecotoxicology, 18: 939–951.
Razmara P., Heyrati Peykan F. and Dorafshan S. 2014. Effect of silver nanoparticles on some hematological indices of rainbow catfish (Pangasius hypophthalmus). Journal of Cell and Tissue, 5: 263–272.
Riley L.G., Hirano T. and Grau E.G. 2003. Effects of transfer from seawater to fresh water on the growth hormone/insulin-like growth factor-I axis and prolactin in the tilapia, Oreochromis mossambicus. Comparative Biochemistry and Physiology (B), 136: 647–655.
Rubio V.C., Sanchez-Vazquez F.J. and Madrid J.A. 2005. Effects of salinity on food intake and macronutrient selection in European sea bass. Physiology and Behavior, 85: 333–339.
Saikia S.K. and Das D.N. 2009. Feeding ecology of common carp (Cyprinus carpio L.) in a rice-fish culture system of the Apatani plateau (Arunachal Pradesh, India). Aquatic Ecology, 43: 559–568.
Sanchez W., Palluel O., miunier L., Coquery M., Porcher J.M. and Ait-Aissa S. 2005. Copper-induced oxidative stress in three-spined stickleback, relationship with hepatic metal levels. Environmental Toxicology and Pharmacology, 19: 177–183.
Shah S.L. and Altindag A. 2005. Effects of heavy metal accumulation on the 96-h LC50 values in tench Tinca tinca L., 1758. Turkish Journal of Veterinary, 29: 139–144.
Sondi I. and Salopek-Sondi B. 2004. Silver nanoparticles as antimicrobial agent: A case study on E. coli as a model for Gram-negative bacteria. Journal of Colloid and Interface Science, 275: 177–182.
Stoskopf M.A. 1993. Fish Medicine. Sounders Company, USA. 882P.
Tassinari R., Cubadda F., Moracci G., Aureli F., D'Amato M., Valeri M., Berardis B., Raggi A., Mantovani A., Passeri D., Rossi M. and Maranghi F. 2014. Oral, short-term exposure to titanium dioxide nanoparticles in Sprague-Dawley rat: Focus on reproductive and endocrine systems and spleen. Nanotoxicology, 8: 654–662.
Thrall M.A., Weiser G., Allison R.W. and Campbell T.W. 2012. Veterinary Hematology and Clinical Chemistry. Wiley-Blackwell, USA. 784P.
TRC. 1984. OECD guideline for testing a chemicals section 2, on biotic systems. OECD, France. 39P.
Wood C., Farrell A. and Brauner C. 2012. Fish Physiology: Homeostasis and Toxicology of Essential Metals. Academic Press, USA. 520P.
Younis E.M., Abdel-Warith A.A. and AL-Asgan N.A. 2012. Hematological and enzymatic responses of Nile tilapia, Oreochromis niloticus, during short and long term sub lethal exposure to zine. African Journal of Biotechnology, 11: 4442–4446.