Abstract

Fish contamination by heavy metals, even at low levels, has an adverse effect on human health. Mercury (Hg), cadmium (Cd), and lead (Pb) are the most common heavy metals that contaminate sea foods. Rainbow trout is a fish species which is widely cultured in fresh water regions, e.g. in Yasuj, southwest of Iran. Heavy metal contamination was measured in three different culture areas (A, B, and C), with three different feed pellets used in Yasuj farms (I, II, and III). The sampling was conducted during February-April 2018 and the metals were measured using cold vapour atomic absorption with a Perkin Elmer 4100. The mean values of Hg, Cd, and Pb levels in the muscular tissue of the samples were 0.022, 0.105, and 1.07 mg/kg, respectively. Concentrations of Hg and Cd in edible tissues of rainbow trout were lower than the permitted values set by the WHO, the FDA, and the EC. The samples fed on mixture pellets III showed a significantly higher Hg content and a lower concentration of Cd in the muscle tissue compared to those given feed mixtures I and II (P < 0.05). Pearson correlation tests revealed significant correlations between the Cd and Pb concentrations and the weight of the fish samples (r = –0.519, r = –0.580). The lowest Cd concentration (0.076 mg/kg^–1) was found in site A located close to the spring and not polluted by sewage from urban or rural areas. The study showed a correlation between the concentration of heavy metals in the fish samples and their weight, the degree of pollution, and the feeding mixture used in the farms.

Keywords

Rainbow trout, heavy metals, mercury, cadmium, lead

REFERENCES

1. Ibrahim F, Halttunen T, Tahvonen R, Salminen S. Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Canadian Journal of Microbiology. 2006;52(9):877–885. DOI: https://doi.org/10.1139/w06-043.
2. Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Walker P, et al. Aquaculture practices and potential human health risks: Current knowledge and future priorities. Environment International. 2008;34(8):1215–1226. DOI: https://doi.org/10.1016/j.envint.2008.04.009.
3. Gu Y-G, Lin Q, Wang X-H, Du F-Y, Yu Z-L, Huang H-H. Heavy metal concentrations in wild fishes captured from the South China Sea and associated health risks. Marine Pollution Bulletin. 2015;96(1–2):508–512. DOI: https://doi.org/10.1016/j.marpolbul.2015.04.022.
4. Saha N, Mollah MZI, Alam MF, Rahman MS. Seasonal investigation of heavy metals in marine fishes captured from the Bay of Bengal and the implications for human health risk assessment. Food Control. 2016;70:110–118. DOI: https://doi.org/10.1016/j.foodcont.2016.05.040.
5. Chen M, Zeng GM, Zhang JC, Xu P, Chen AW, Lu LH. Global Landscape of Total Organic Carbon, Nitrogen and Phosphorus in Lake Water. Scientific Reports. 2015;5:7. DOI: https://doi.org/10.1038/srep15043.
6. Saei-Dehkordi SS, Fallah AA. Determination of copper, lead, cadmium and zinc content in commercially valuable fish species from the Persian Gulf using derivative potentiometric stripping analysis. Microchemical Journal. 2011;98(1):156–162. DOI: https://doi.org/10.1016/j.microc.2011.01.001.
7. Fornshell G. Rainbow trout – Challenges and solutions. Reviews in Fisheries Science. 2002;10(3–4):545–557. DOI: https://doi.org/10.1080/20026491051785.
8. Kalbassi MR, Abdollahzadeh E, Salari-Joo H. A review on aquaculture development in Iran. Ecopersia. 2013;1(2): 159–178.
9. Ebadzadeh MM. Agriculture. Economic aspects – Iran. Tehran: Ministry of Agriculture, Deputy Director of Planning and Economics; 2016. pp. 117–127.
10. Castro-Gonzalez MI, Mendez-Armenta M. Heavy metals: Implications associated to fish consumption. Environmental Toxicology and Pharmacology. 2008;26(3):263–271. DOI: https://doi.org/10.1016/j.etap.2008.06.001.
11. Demirak A, Yilmaz F, Tuna AL, Ozdemir N. Heavy metals in water, sediment and tissues of Leuciscus cephalus from a stream in southwestern Turkey. Chemosphere. 2006;63(9):1451–1458. DOI: https://doi.org/10.1016/j.chemosphere.2005.09.033.
12. Piper D, Restrepo JFC. Lead and Cadmium: Priorities for action from UNEP’s perspective for addressing risks posed by these two heavy metals. 16th International Conference on Heavy Metals in the Environment (ICHMET); 2012; Rome. Rome: EDP Sciences; 2013. DOI: https://doi.org/10.1051/e3sconf/20130130004.
13. Cadmium dietary exposure in the European population. EFSA Journal. 2012;10(1):2551. DOI: https://doi.org/10.2903/j.efsa.2012.2551.
14. Benefice E, Luna-Monrroy S, Lopez-Rodriguez R. Fishing activity, health characteristics and mercury exposure of Amerindian women living alongside the Beni River (Amazonian Bolivia). International Journal of Hygiene and Environmental Health. 2010;213(6):458–464. DOI: https://doi.org/10.1016/j.ijheh.2010.08.010.
15. Burger J, Jeitner C, Gochfeld M. Locational Differences in Mercury and Selenium Levels in 19 Species of Saltwater Fish from New Jersey. Journal of Toxicology and Environmental Health-Part A: Current Issues. 2011;74(13): 863–874. DOI: https://doi.org/10.1080/15287394.2011.570231.
16. Fallah AA, Saei-Dehkordi SS, Nematollahi A, Jafari T. Comparative study of heavy metal and trace element accumulation in edible tissues of farmed and wild rainbow trout (Oncorhynchus mykiss) using ICP-OES technique. Microchemical Journal. 2011;98(2):275–279. DOI: https://doi.org/10.1016/j.microc.2011.02.007.
17. Hosseini M, Nabavi SMB, Nabavi SN, Pour NA. Heavy metals (Cd, Co, Cu, Ni, Pb, Fe, and Hg) content in four fish commonly consumed in Iran: risk assessment for the consumers. Environmental Monitoring and Assessment. 2015;187(5). DOI: https://doi.org/10.1007/s10661-015-4464-z.
18. Moradi S, Nowzari H, Farhadian M. Assessment of cadmium and lead in the water and trout fish (Salmo trutta) of Zayandehroud River, a case study of Zarinshahr rice farms, Isfahan. Iranian Journal of Fisheries Sciences. 2017;16(1):188–199.
19. Chatta AM, Khan MN, Mirza ZS, Ali A. Heavy metal (cadmium, lead, and chromium) contamination in farmed fish: a potential risk for consumers’ health. Turkish Journal of Zoology. 2016;40(2):248–256. DOI: https://doi.org/10.3906/zoo-1506-1.
20. Nevarez M, Leal LO, Moreno M. Estimation of Seasonal Risk Caused by the Intake of Lead, Mercury and Cadmium through Freshwater Fish Consumption from Urban Water Reservoirs in Arid Areas of Northern Mexico. International Journal of Environmental Research and Public Health. 2015;12(2):1803–1816. DOI: https://doi.org/10.3390/ijerph120201803.
21. Turkmen M, Ciminli C. Determination of metals in fish and mussel species by inductively coupled plasma-atomic emission spectrometry. Food Chemistry. 2007;103(2):670–675. DOI: https://doi.org/10.1016/j.foodchem.2006.07.054.
22. Monikh FA, Safahieh A, Savari A, Doraghi A. Heavy metal concentration in sediment, benthic, benthopelagic, and pelagic fish species from Musa Estuary (Persian Gulf). Environmental Monitoring and Assessment. 2013;185(1): 215–222. DOI: https://doi.org/10.1007/s10661-012-2545-9.
23. Navarro MC, Perez-Sirvent C, Martinez-Sanchez MJ, Vidal J, Marimon J. Lead, cadmium and arsenic bloavallability in the abandoned mine site of Cabezo Rajao (Murcia, SE Spain). Chemosphere. 2006;63(3):484–489. DOI: https://doi.org/10.1016/j.chemosphere.2005.08.017.
24. Jiang DS, Hu ZZ, Liu F, Zhang RF, Duo B, Fu JJ, et al. Heavy metals levels in fish from aquaculture farms and risk assessment in Lhasa, Tibetan Autonomous Region of China. Ecotoxicology. 2014;23(4):577–583. DOI: https://doi.org/10.1007/s10646-014-1229-3.
25. Barnes DG, Dourson M, Dourson M, Preuss P, Barnes DG, Bellin J, et al. Reference dose (RFD): description and use in health risk assessments. Regulatory Toxicology and Pharmacology. 1988;8(4):471–486. DOI: https://doi.org/10.1016/0273-2300(88)90047-5.
26. Kelly BC, Ikonomou MG, Higgs DA, Oakes J, Dubetz C. Mercury and other trace elements in farmed and wild salmon from British Columbia, Canada. Environmental Toxicology and Chemistry. 2008;27(6):1361–1370. https://doi.org/10.1897/07-527.1.
27. Evaluation of certain food additives and contaminants. World Health Organization technical report series; 2011;(966). 109 p.
28. Leonard B. Fish and Fishery Products: Hazards and Controls Guidance. DIANE Publishing; 2011. 468 p.
29. Commission regulation (EC) No 1881/2006 of 19 December 2006 Setting maximum levels for certain contaminants in foodstuffs [Internet]. [cited 2019 April 10]. Available from: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32006R1881&from=EN.
30. Evaluation of certain food additive and contaminants (Section 5.2 Lead). World Health Organization technical report series; 2011(960). pp. 162–177.
31. Zhilin AY, Plotitsyna NF, Lapteva AM, editors. Heavy Metals in Commercial Fish from the Barents Sea (Winter 2011). 16th International Conference on Heavy Metals in the Environment (ICHMET); 2012; Rome. Rome: EDP Sciences; 2013. DOI: https://doi.org/10.1051/e3sconf/20130111008.
32. Ahmad A, Shuhaimi-Othman M. Heavy Metal Concentrations in Sediments and Fishes from Lake Chini, Pahang, Malaysia. Journal of Biological Sciences. 2010;10(2):93–100. DOI: https://doi.org/10.3923/jbs.2010.93.100.
33. Majlesi M, Khazaei Y, Berizi E, Sharifpour E. The Concentration of Mercury, Cadmium and Lead in Muscular Tissue of Fishes in Khersan River. International Journal of Nutrition Sciences. 2017;2(3):2–9 .
34. Mortazavi A, Hatamikia M, Bahmani M, Hassanzadazar H. Heavy Metals (Mercury, Lead and Cadmium) Determination in 17 Species of Fish Marketed in Khorramabad City, West of Iran. Journal of Chemical Health Risks. 2016;6(1).
35. Papagiannis I, Kagalou I, Leonardos J, Petridis D, Kalfakakou V. Copper and zinc in four freshwater fish species from Lake Pamvotis (Greece). Environment International. 2004;30(3):357–362. DOI: https://doi.org/10.1016/j.envint.2003.08.002.
36. Bat L, Şahin F, Öztekin A, Arici E, Yardim Ö. Assessment of Cd, Hg, Pb, Cu and Zn amounts in muscles of Cyprinus carpio from Karasu Stream, Sinop. Current Agriculture Research Journal. 2019;7(2). DOI: https://doi.org/10.12944/CARJ.7.2.05.
37. Bat L, Yardım Ö, Özteki̇n A, Şahi̇n. F. Bioaccumulation of Metals in Fish from Sarikum Lake. Aquatic Science and Technology. 2019;7(1):1–7. DOI: https://doi.org/10.5296/ast.v7i1.13456.
38. Reyahi-Khoram M, Setayesh-Shiri F, Cheraghi M. Study of the heavy metals (Cd and Pb) content in the tissues of rainbow trouts from Hamedan coldwater fish farms. Iranian Journal of Fisheries Sciences. 2016;15(2):858–869.
39. Bat L, Oztekin A, Yardim O. Metal levels in large sea trout from Sinop fish market. Fresenius Environmental Bulletin. 2018;27(12):8505–8508.
40. Salaramoli J, Salamat N, Razavilar V, Najafpour Sh, Aliesfahani T. A Quantitative Analysis of Lead, Mercury and Cadmium Intake by Three Commercial Aquatics, Hypophthalmichthys Molitrix, Onchorhynchus Mykiss (Walbaum) and Fenneropenaeus Indicus. World Applied Sciences Journal. 2012;16(4):583–588.
41. Wagner A, Boman J. Biomonitoring of trace elements in muscle and liver tissue of freshwater fish. Spectrochimica Acta Part B: Atomic Spectroscopy. 2003;58(12):2215–2226. DOI: https://doi.org/10.1016/j.sab.2003.05.003.
42. Can E, Yabanli M, Kehayias G, Aksu O, Kocabas M, Demir V, et al. Determination of Bioaccumulation of Heavy Metals and Selenium in Tissues of Brown Trout Salmo trutta macrostigma (Dumeril, 1858) from Munzur Stream, Tunceli, Turkey. Bulletin of Environmental Contamination and Toxicology. 2012;89(6):1186–1189. DOI: https://doi.org/10.1007/s00128-012-0824-3.
43. Solgi E, Beigzadeh-Shahraki F. Accumulation and Human Health Risk of Heavy Metals in Cultured Rainbow Trout (Oncorhynchus mykiss) Form Different Fish Farms of Eight Cities of Chaharmahal and Bakhtiari Province, Iran. Thalassas. 2019;35(1):305–317. DOI: https://doi.org/10.1007/s41208-019-0123-4.
44. Mohammadi M, Sary AA, Khodadadi M. Accumulation variations of selected heavy metals in Barbus xanthopterus in Karoon and Dez rivers of Khuzestan, Iran. Iranian Journal of Fisheries Sciences. 2012;11(2):372–382.
45. Sivaperumal P, Sankar TV, Nair PGV. Heavy metal concentrations in fish, shellfish and fish products from internal markets of India vis-a-vis international standards. Food Chemistry. 2007;102(3):612–620. DOI: https://doi.org/10.1016/j.foodchem.2006.05.041.
46. Shakir HA, Qazi JI, Chaudhry AS. Assessing Human Health Risk of Metal Accumulations in a wild carp fish from Selected Sites of a River Loaded with Municipal and Industrial Wastes. International Journal of Environmental Research. 2015;9(2):545–552.
47. Jabeen F, Chaudhry AS. Monitoring trace metals in different tissues of Cyprinus carpio from the Indus River in Pakistan. Environmental Monitoring and Assessment. 2010;170(1–4):645–656. DOI: https://doi.org/10.1007/s10661-009-1263-4.
48. Emara MM, Farag RS, Dawah AMA, Fathi M. Assessment of heavy metals concentration in water and edible Nile Tilapia (Oreochromis niloticus) from two fish farms irrigated with different water sources, Egypt. International Journal of Environment. 2015;4(1):108–115.
49. Yilmaz AB. Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environmental Research. 2003;92(3):277–281. DOI: https://doi.org/10.1016/s0013-9351(02)00082-8.
50. Majlesi M, Pashangeh S, Salehi SO, Berizi E. Human Health Risks from Heavy Metals in Fish of a Fresh Water River in Iran. International Journal of Nutrition Sciences 2018;3(3):2–8.
51. Miri M, Akbari E, Amrane A, Jafari SJ, Eslami H, Hoseinzadeh E, et al. Health risk assessment of heavy metal intake due to fish consumption in the Sistan region, Iran. Environmental Monitoring and Assessment. 2017;189(11). DOI: https://doi.org/10.1007/s10661-017-6286-7.
52. Yilmaz F, Ozdemir N, Demirak A, Tuna AL. Heavy metal levels in two fish species Leuciscus cephalus and Lepomis gibbosus. Food Chemistry. 2007;100(2):830–835. DOI: https://doi.org/10.1016/j.foodchem.2005.09.020.
53. Commission regulation (EU) 582/2016 of 15 April 2016, amending Regulation (EC) No 333/2007 as regards the analysis of inorganic arsenic, lead and polycyclic aromatic hydrocarbons and certain performance criteria for analysis. Euratom. 2016;3–6.
54. Canli M, Furness RW. Mercury and cadmium uptake from seawater and from food by the Norway lobster Nephrops norvegicus. Environmental Toxicology and Chemistry. 1995;14(5):819–828. DOI: https://doi.org/10.1002/etc.5620140512.
55. Geyer HJ, Scheunert I, Bruggemann R, Steinberg C, Korte F, Kettrup A. QSAR for organic-chemical bioconcentration in Daphnia, algae, and mussels. Science of the Total Environment. 1991;109:387–394. DOI: https://doi.org/10.1016/0048-9697(91)90193-i.
56. Canli M, Atli G. The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environmental Pollution. 2003;121(1):121–136. DOI: https://doi.org/10.1016/s0269-7491(02)00194-x.
57. Varol M, Kaya GK, Alp A. Heavy metal and arsenic concentrations in rainbow trout (Oncorhynchus mykiss) farmed in a dam reservoir on the Firat (Euphrates) River: Risk-based consumption advisories. Science of the Total Environment. 2017;599:1288–1296. DOI: https://doi.org/10.1016/j.scitotenv.2017.05.052.
58. Liu HL, Li LQ, Yin CQ, Shan BQ. Fraction distribution and risk assessment of heavy metals in sediments of Moshui Lake. Journal of Environmental Sciences. 2008;20(4):390–397. DOI: https://doi.org/10.1016/s1001-0742(08)62069-0.
59. Rainbow PS. Trace metal concentrations in aquatic invertebrates: why and so what? Environmental Pollution. 2002;120(3):497–507. DOI: https://doi.org/10.1016/s0269-7491(02)00238-5.
60. Nussey G, van Vuren JHJ, du Preez HH. Bioaccumulation of chromium, manganese, nickel and lead in the tissues of the moggel, Labeo umbratus (Cyprinidae), from Witbank Dam, Mpumalanga. Water Sa. 2000;26(2):269–284.
61. Widianarko B, Van Gestel CAM, Verweij RA, Van Straalen NM. Associations between trace metals in sediment, water, and guppy, Poecilia reticulata (Peters), from urban streams of Semarang, Indonesia. Ecotoxicology and Environmental Safety. 2000;46(1):101–107. DOI: https://doi.org/10.1006/eesa.1999.1879.
62. Douben PE. Lead and cadmium in stone loach (Noemacheilus barbatulus L.) from three rivers in Derbyshire. Ecotoxicology and Environmental Safety. 1989;18(1):35–58.
63. Poorbagher H, Hosseini SV, Hosseini SM, Aflaki F, Regenstein JM. Metal accumulation in Caspian sturgeons with different feeding niches, condition factor, body size and age. Microchemical Journal. 2017;132:43–48. DOI: https://doi.org/10.1016/j.microc.2017.01.003.
64. Fagerstrom T. Body-weight, metabolic-rate, and trace substance turnover in animals. Oecologia. 1977;29(2):99–104. DOI: https://doi.org/10.1007/bf00345790.
65. Newman MC, Doubet DK. Size-dependence of mercury(ii) accumulation kinetics in the mosquitofish, Gambusia affinis (Baird and Girard). Archives of Environmental Contamination and Toxicology. 1989;18(6):819–825. DOI: https://doi.org/10.1007/bf01160295.
66. Farkas A, Salanki J, Specziar A. Age- and size-specific patterns of heavy metals in the organs of freshwater fish Abramis brama L. populating a low-contaminated site. Water Research. 2003;37(5):959–964. DOI: https://doi.org/10.1016/s0043-1354(02)00447-5.
67. Hellawell JM. Biological indicators of freshwater pollution and environmental management. Springer Netherlands; 2012. 546 p.
68. Marmulla G, Rosch R. Maximum daily ration of juvenile fish fed on living natural zooplankton. Journal of Fish Biology. 1990;36(6):789–801. DOI: https://doi.org/10.1111/j.1095-8649.1990.tb05628.x.
69. Bustamante P, Bocher P, Cherel Y, Miramand P, Caurant F. Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands. Science of the Total Environment. 2003;313(1–3):25–39. DOI: https://doi.org/10.1016/S0048-9697(03)00265-1.
70. Yi YJ, Wang ZY, Zhang K, Yu GA, Duan XH. Sediment pollution and its effect on fish through food chain in the Yangtze River. International Journal of Sediment Research. 2008;23(4):338–347. DOI: https://doi.org/10.1016/s1001-6279(09)60005-6.