Polycyclic aromatic hydrocarbons and potentially toxic elements in seafood from the Persian Gulf: presence, trophic transfer, and chronic intake risk assessment

  • Razegheh Akhbarizadeh
  • Farid MooreEmail author
  • Behnam Keshavarzi
Original Paper


High bioavailability of man-made pollutants in marine environments raises serious concern regarding the safety of seafood. In the present study, the presence, trophic transfer, and risks of polycyclic aromatic hydrocarbons (PAHs), and potentially toxic elements (PTEs) in 170 benthic marine organisms (87 prawn; 28 crab; 55 fish) from the Persian Gulf were investigated. Among investigated species, E. coioides displayed the lowest level of metal pollution index (MPI), while P. armatus and P. semisulcatus showed the highest level of MPI and total PAHs, respectively. Principal component biplot exhibited a significant association of PTEs (except Hg) and PAHs in less motile benthic species. The results of trophic transfer investigation revealed that PTEs (except Hg) and PAHs were not biomagnified in the studied organisms through diet. However, Hg biomagnification factors greater than 1 indicated trophic transfer of mercury. In order to gain nutritional benefits of seafood, consumption of two fish/prawn meals/week for adults (except vulnerable groups such as pregnant women) and one fish/prawn meals/week for children is recommended. However, lifelong consumption of crabs (P. armatus) may threaten human health. In addition, the maximum allowable fish consumption rate (CRlim) for studied fish is 120 g fish/day for adults and 30 g fish/day for children. In the case of prawns, the safe dose is 30 and 10 g prawns/day for adults and children, respectively.


Polycyclic aromatic hydrocarbons (PAHs) Potentially toxic elements (PTEs) Combined exposure Trophic transfer Seafood safety 



This research was financially supported by the Iran National Science foundation Grant No. 96006051 to which we are indebted. The authors would also like to extend their gratitude to the medical geology research center of Shiraz University and National Elites Foundation of Islamic Republic of Iran for logistic support.

Supplementary material

10653_2019_343_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 29 kb)


  1. Abdolahpur Monikh, F., Safahieh, A., Savari, A., Ronagh, M. T., & Doraghi, A. (2013). The relationship between heavy metal (Cd Co, Cu, Ni and Pb) levels and the size of benthic, benthopelagic and pelagic fish species, Persian Gulf. Bulletin of Environment Contamination and Toxicology, 90(6), 691–696. Scholar
  2. Akhbarizadeh, R., Moore, F., & Keshavarzi, B. (2018). Investigating a probable relationship between microplastics and potentially toxic elements in fish muscles from northeast of Persian Gulf. Environmental Pollution, 232, 154–163.CrossRefGoogle Scholar
  3. Akhbarizadeh, R., Moore, F., Keshavarzi, B., & Moeinpour, A. (2017). Microplastics and potentially toxic elements in coastal sediments of Iran’s main oil terminal (Khark Island). Environmental Pollution, 220(Pt A), 720–731. Scholar
  4. Alamdar, A., Eqani, S., Hanif, N., Ali, S. M., Fasola, M., Bokhari, H., et al. (2017). Human exposure to trace metals and arsenic via consumption of fish from river Chenab, Pakistan and associated health risks. Chemosphere, 168, 1004–1012. Scholar
  5. AL-Khion, D. D., Al-Ali, B. S., Al-Nagar, G., Al-Saad, H. T., & Al-Anber, L. J. (2016). Polycyclic aromatic hydrocarbons in some fishes from the Iraqi marine waters. International Journal of Science and Research (IJSR), 7(1), 1911–1917.Google Scholar
  6. Ayas, D., & Özogul, Y. (2011). The chemical composition of sexually mature blue swimmer crab (Portunus pelagicus, Linnaeus 1758) in the Mersin Bay. Journal of FisheriesSciences. com, 5(4), 308.Google Scholar
  7. Bandowe, B. A., Bigalke, M., Boamah, L., Nyarko, E., Saalia, F. K., & Wilcke, W. (2014). Polycyclic aromatic compounds (PAHs and oxygenated PAHs) and trace metals in fish species from Ghana (West Africa): Bioaccumulation and health risk assessment. Environment International, 65, 135–146. Scholar
  8. Barhoumi, B., El Megdiche, Y., Clérandeau, C., Ameur, W. B., Mekni, S., Bouabdallah, S., et al. (2016). Occurrence of polycyclic aromatic hydrocarbons (PAHs) in mussel (Mytilus galloprovincialis) and eel (Anguilla anguilla) from Bizerte lagoon, Tunisia, and associated human health risk assessment. Continental Shelf Research, 124, 104–116. Scholar
  9. Bastami, K. D., Afkhami, M., Ehsanpour, M., Kazaali, A., Mohammadizadeh, M., Haghparast, S., et al. (2013). Polycyclic aromatic hydrocarbons in the coastal water, surface sediment and mullet Liza klunzingeri from northern part of Hormuz strait (Persian Gulf). Marine Pollution Bulletin, 76(1–2), 411–416. Scholar
  10. Bastami, K. D., Afkhami, M., Mohammadizadeh, M., Ehsanpour, M., Chambari, S., Aghaei, S., et al. (2015). Bioaccumulation and ecological risk assessment of heavy metals in the sediments and mullet Liza klunzingeri in the northern part of the Persian Gulf. Marine Pollution Bulletin, 94(1–2), 329–334.CrossRefGoogle Scholar
  11. Batvari, B. P. D., Sivakumar, S., Shanthi, K., Lee, K.-J., Oh, B.-T., Krishnamoorthy, R., et al. (2016). Heavy metals accumulation in crab and prawns from Pulicat lake, north Chennai coastal region, southeast coast of India. Toxicology and Industrial Health, 32(1), 1–6.CrossRefGoogle Scholar
  12. Benali, I., Boutiba, Z., Grandjean, D., de Alencastro, L. F., Rouane-Hacene, O., & Chevre, N. (2017). Spatial distribution and biological effects of trace metals (Cu, Zn, Pb, Cd) and organic micropollutants (PCBs, PAHs) in mussels Mytilus galloprovincialis along the Algerian west coast. Marine Pollution Bulletin, 115(1–2), 539–550. Scholar
  13. Benson, N. U., Anake, W. U., Adedapo, A. E., Fred-Ahmadu, O. H., & Eke, K. P. (2017). Polycyclic aromatic hydrocarbons in imported Sardinops sagax: Levels and health risk assessments through dietary exposure in Nigeria. Journal of Food Composition and Analysis, 57, 109–116.CrossRefGoogle Scholar
  14. Bibak, M., Sattari, M., Agharokh, A., Tahmasebi, S., & Imanpour Namin, J. (2018). Assessing some heavy metals pollutions in sediments of the northern Persian Gulf (Bushehr province). Environmental Health Engineering and Management, 5(3), 175–179.CrossRefGoogle Scholar
  15. Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), 911–917.CrossRefGoogle Scholar
  16. Bu-Olayan, A., & Thomas, B. (2005). Toxicity and bioaccumulation of heavy metals in mullet fish Liza klunzingeri (Mugilidae: Perciformes). Chemistry and Ecology, 21(3), 191–197.CrossRefGoogle Scholar
  17. Burgos-Nunez, S., Navarro-Frometa, A., Marrugo-Negrete, J., Enamorado-Montes, G., & Urango-Cardenas, I. (2017). Polycyclic aromatic hydrocarbons and heavy metals in the Cispata Bay, Colombia: A marine tropical ecosystem. Marine Pollution Bulletin, 120(1–2), 379–386. Scholar
  18. Cappello, T., Giannetto, A., Parrino, V., De Marco, G., Mauceri, A., & Maisano, M. (2018). Food safety using NMR-based metabolomics: Assessment of the Atlantic bluefin tuna, Thunnus thynnus, from the Mediterranean Sea. Food and Chemical Toxicology, 115, 391–397. Scholar
  19. Cheung, K., Leung, H., Kong, K., & Wong, M. (2007). Residual levels of DDTs and PAHs in freshwater and marine fish from Hong Kong markets and their health risk assessment. Chemosphere, 66(3), 460–468.CrossRefGoogle Scholar
  20. Copat, C., Arena, G., Fiore, M., Ledda, C., Fallico, R., Sciacca, S., et al. (2013). Heavy metals concentrations in fish and shellfish from eastern Mediterranean Sea: Consumption advisories. Food and Chemical Toxicology, 53, 33–37. Scholar
  21. Copat, C., Grasso, A., Fiore, M., Cristaldi, A., Zuccarello, P., Signorelli, S. S., et al. (2018). Trace elements in seafood from the Mediterranean sea: An exposure risk assessment. Food and Chemical Toxicology, 115, 13–19. Scholar
  22. Corsolini, S., & Sara, G. (2017). The trophic transfer of persistent pollutants (HCB, DDTs, PCBs) within polar marine food webs. Chemosphere, 177, 189–199. Scholar
  23. de Mora, S., Fowler, S. W., Wyse, E., & Azemard, S. (2004). Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman. Marine Pollution Bulletin, 49(5), 410–424.CrossRefGoogle Scholar
  24. Devier, M.-H., Augagneur, S., Budzinski, H., Le Menach, K., Mora, P., Narbonne, J.-F., et al. (2005). One-year monitoring survey of organic compounds (PAHs, PCBs, TBT), heavy metals and biomarkers in blue mussels from the Arcachon Bay, France. Journal of Environmental Monitoring, 7(3), 224–240.CrossRefGoogle Scholar
  25. Ejike, C. E., Mbaraonye, O. E., & Enyinnaya, E. R. (2015). Fatty acid saturation profiles and lipid contents of muscles from six popular culinary fish species sold in Umuahia, Nigeria. Journal of Medical Nutrition and Nutraceuticals, 4(2), 91.CrossRefGoogle Scholar
  26. Ferrante, M., Zanghi, G., Cristaldi, A., Copat, C., Grasso, A., Fiore, M., et al. (2018). PAHs in seafood from the Mediterranean Sea: An exposure risk assessment. Food and Chemical Toxicology, 115, 385–390. Scholar
  27. Francioni, E., de Wagener, A., de Scofield, A. D. L., Depledge, M., Cavalier, B., Sette, C., et al. (2007). Polycyclic aromatic hydrocarbon in inter-tidal mussel Perna perna: Space–time observations, source investigation and genotoxicity. Science of the Total Environment, 372(2–3), 515–531.CrossRefGoogle Scholar
  28. Froese, R., & Pauly, D. J. U. W. F. O. A. (2012). FishBase World Wide Web electronic publication, Version (09/2010). 1.Google Scholar
  29. Gagnon, M. M., Baker, J. K., Long, S. M., Hassell, K. L., & Pettigrove, V. J. (2016). Contaminant (PAHs, OCs, PCBs and trace metals) concentrations are declining in axial tissue of sand flathead (Platycephalus bassensis) collected from an urbanised catchment (Port Phillip Bay, Australia). Marine Pollution Bulletin, 109(1), 661–666. Scholar
  30. Ghaeni, M., Pour, N. A., & Hosseini, M. (2015). Bioaccumulation of polychlorinated biphenyl (PCB), polycyclic aromatic hydrocarbon (PAH), mercury, methyl mercury, and arsenic in blue crab Portunus segnis from Persian Gulf. Environmental Monitoring and Assessment, 187(5), 253.CrossRefGoogle Scholar
  31. Gu, Y. G., Lin, Q., Wang, X. H., Du, F. Y., Yu, Z. L., & Huang, H. H. (2015). Heavy metal concentrations in wild fishes captured from the South China Sea and associated health risks. Marine Pollution Bulletin, 96(1–2), 508–512. Scholar
  32. Hao, Y., Chen, L., Zhang, X., Zhang, D., Zhang, X., Yu, Y., et al. (2013). Trace elements in fish from Taihu Lake, China: Levels, associated risks, and trophic transfer. Ecotoxicology and Environmental Safety, 90, 89–97.CrossRefGoogle Scholar
  33. Heidarieh, M., Maragheh, M. G., Shamami, M. A., Behgar, M., Ziaei, F., & Akbari, Z. (2013). Evaluate of heavy metal concentration in prawn (Penaeus semisulcatus) and crab (Portunus pelagicus) with INAA method. SpringerPlus, 2(1), 72.CrossRefGoogle Scholar
  34. Jaafarzadeh Haghighi Fard, N., Ravanbakhsh, M., Ramezani, Z., Ahmadi, M., Angali, K. A., & Javid, A. Z. (2015). Determination of mercury and vanadium concentration in Johnius belangerii (C) fish in Musa estuary in Persian Gulf. Marine Pollution Bulletin, 97(1–2), 499–505. Scholar
  35. Jacobs, S., Sioen, I., Marques, A., & Verbeke, W. (2018). Consumer response to health and environmental sustainability information regarding seafood consumption. Environmental Research, 161, 492–504. Scholar
  36. Josileen, J. J. C. (2011). Food and feeding of the blue swimmer crab, Portunus pelagicus (Linnaeus, 1758)(Decapoda, Brachyura) along the coast of Mandapam, Tamil Nadu, India. Crustaceana, 84(10), 1169–1180.CrossRefGoogle Scholar
  37. Ke, C. L., Gu, Y. G., Liu, Q., Li, L. D., Huang, H. H., Cai, N., et al. (2017). Polycyclic aromatic hydrocarbons (PAHs) in wild marine organisms from South China Sea: Occurrence, sources, and human health implications. Marine Pollution Bulletin, 117(1–2), 507–511. Scholar
  38. Kelly, B. C., Ikonomou, M. G., Higgs, D. A., Oakes, J., & Dubetz, C. (2008). Mercury and other trace elements in farmed and wild salmon from British Columbia, Canada. Environmental Toxicology and Chemistry, 27(6), 1361–1370.CrossRefGoogle Scholar
  39. Khoshnoud, M. J., Mobini, K., Javidnia, K., Hosseinkhezri, P., & Aeen Jamshid, K. (2011). Heavy metals (Zn, Cu, Pb, Cd and Hg) contents and fatty acids ratios in two fish species (Scomberomorus commerson and Otolithes ruber) of the Persian Gulf. Iranian Journal of Pharmaceutical Sciences, 7(3), 191–196.Google Scholar
  40. Leung, H., Leung, A., Wang, H., Ma, K., Liang, Y., Ho, K., et al. (2014). Assessment of heavy metals/metalloid (As, Pb, Cd, Ni, Zn, Cr, Cu, Mn) concentrations in edible fish species tissue in the Pearl River Delta (PRD), China. Marine Pollution Bulletin, 78(1–2), 235–245.CrossRefGoogle Scholar
  41. Lundebye, A. K., Lock, E. J., Rasinger, J. D., Nostbakken, O. J., Hannisdal, R., Karlsbakk, E., et al. (2017). Lower levels of Persistent Organic Pollutants, metals and the marine omega 3-fatty acid DHA in farmed compared to wild Atlantic salmon (Salmo salar). Environmental Research, 155, 49–59. Scholar
  42. Mackay, D., & Fraser, A. (2000). Bioaccumulation of persistent organic chemicals: mechanisms and models. Environmental Pollution, 110(3), 375–391.CrossRefGoogle Scholar
  43. Mackintosh, C. E., Maldonado, J., Hongwu, J., Hoover, N., Chong, A., Ikonomou, M. G., et al. (2004). Distribution of phthalate esters in a marine aquatic food web: Comparison to polychlorinated biphenyls. Environmental Science and Technology, 38(7), 2011–2020.CrossRefGoogle Scholar
  44. Mirza, R., Mohammadi, M., Sohrab, A. D., Safahieh, A., Savari, A., Hajeb, P., et al. (2012). Polycyclic aromatic hydrocarbons in seawater, sediment, and rock oyster Saccostrea cucullata from the northern part of the Persian Gulf (Bushehr Province). Water, Air, and Soil pollution, 223(1), 189–198.CrossRefGoogle Scholar
  45. Murillo, E., Rao, K., & Durant, A. A. (2014). The lipid content and fatty acid composition of four eastern central Pacific native fish species. Journal of Food Composition and Analysis, 33(1), 1–5.CrossRefGoogle Scholar
  46. Naji, A., Khan, F. R., & Hashemi, S. H. (2016). Potential human health risk assessment of trace metals via the consumption of marine fish in Persian Gulf. Marine Pollution Bulletin, 109(1), 667–671. Scholar
  47. Neori, A., & Nobre, A. M. (2012). Relationship between trophic level and economics in aquaculture. Aquaculture Economics & Management, 16(1), 40–67.CrossRefGoogle Scholar
  48. Nunez, R., Garcia, M. A., Alonso, J., & Melgar, M. J. (2018). Arsenic, cadmium and lead in fresh and processed tuna marketed in Galicia (NW Spain): Risk assessment of dietary exposure. Science of the Total Environment, 627, 322–331. Scholar
  49. Olmedo, P., Pla, A., Hernandez, A. F., Barbier, F., Ayouni, L., & Gil, F. (2013). Determination of toxic elements (mercury, cadmium, lead, tin and arsenic) in fish and shellfish samples. Risk assessment for the consumers. Environment International, 59, 63–72. Scholar
  50. Perugini, M., Visciano, P., Manera, M., Zaccaroni, A., Olivieri, V., & Amorena, M. (2014). Heavy metal (As, Cd, Hg, Pb, Cu, Zn, Se) concentrations in muscle and bone of four commercial fish caught in the central Adriatic Sea, Italy. Environmental Monitoring and Assessment, 186(4), 2205–2213. Scholar
  51. Romero-Romero, S., Herrero, L., Fernandez, M., Gomara, B., & Acuna, J. L. (2017). Biomagnification of persistent organic pollutants in a deep-sea, temperate food web. Science of the Total Environment, 605–606, 589–597. Scholar
  52. Saeed, T., Al-Yakoob, S., Al-Hashash, H., & Al-Bahloul, M. (1995). Preliminary exposure assessment for Kuwaiti consumers to polycyclic aromatic hydrocarbons in seafood. Environment International, 21(3), 255–263.CrossRefGoogle Scholar
  53. Saei-Dehkordi, S. S., & Fallah, A. A. (2011). Determination of copper, lead, cadmium and zinc content in commercially valuable fish species from the Persian Gulf using derivative potentiometric stripping analysis. Microchemical Journal, 98(1), 156–162.CrossRefGoogle Scholar
  54. Safaie, M. (2016). Feeding habits of blue swimming crab Portunus segnis (Forskal, 1775) in the northern coastal waters of Iran. Marine Biodiversity Records, 9(1), 68.CrossRefGoogle Scholar
  55. Sarker, S., Vashistha, D., Saha Sarker, M., & Sarkar, A. (2018). DNA damage in marine rock oyster (Saccostrea cucullata) exposed to environmentally available PAHs and heavy metals along the Arabian Sea coast. Ecotoxicology and Environmental Safety, 151, 132–143. Scholar
  56. Schlautman, M. A., Yim, S., Carraway, E. R., Lee, J. H., & Herbert, B. E. J. (2004). Testing a surface tension-based model to predict the salting out of polycyclic aromatic hydrocarbons in model environmental solutions. Water Research, 38(14–15), 3331–3339.CrossRefGoogle Scholar
  57. Sereshk, Z. H., & Bakhtiari, A. R. (2014). Distribution patterns of PAHs in different tissues of annulated sea snake (Hydrophis cyanocinctus) and short sea snake (Lapemis curtus) from the Hara Protected Area on the North Coast of the Persian Gulf, Iran. Ecotoxicology and Environmental Safety, 109, 116–123. Scholar
  58. Sonesten, L. (2003). Fish mercury levels in lakes—Adjusting for Hg and fish-size covariation. Environmental Pollution, 125(2), 255–265.CrossRefGoogle Scholar
  59. Storelli, M. M., Barone, G., Perrone, V. G., & Storelli, A. (2013). Risk characterization for polycyclic aromatic hydrocarbons and toxic metals associated with fish consumption. Journal of Food Composition and Analysis, 31(1), 115–119. Scholar
  60. Taleshi, M. S., Edmonds, J. S., Goessler, W., Ruiz-Chancho, M. J., Raber, G., Jensen, K. B., et al. (2010). Arsenic-containing lipids are natural constituents of sashimi tuna. Environmental Science and Technology, 44(4), 1478–1483.CrossRefGoogle Scholar
  61. Taylor, V., Goodale, B., Raab, A., Schwerdtle, T., Reimer, K., Conklin, S., et al. (2017). Human exposure to organic arsenic species from seafood. Science of the Total Environment, 580, 266–282.CrossRefGoogle Scholar
  62. Tiwari, M., Sahu, S. K., & Pandit, G. G. (2017). Distribution of PAHs in different compartment of creek ecosystem: Ecotoxicological concern and human health risk. Environmental Toxicology and Pharmacology, 50, 58–66. Scholar
  63. Uddin, S., Fowler, S., Behbehani, M., & Metian, M. (2017). 210Po bioaccumulation and trophic transfer in marine food chains in the northern Arabian Gulf. Journal of Environmental Radioactivity, 174, 23–29.CrossRefGoogle Scholar
  64. USEPA. (2000). Guidance for assessing chemical contaminant data for use in fish advisories, Volume 2 risk assessment and fish consumption limits third edition. United States Environmental Protection Agency, EPA 823-B-00-008.Google Scholar
  65. Varol, M., Kaya, G. K., & Alp, A. (2017). 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, 599–600, 1288–1296. Scholar
  66. Varol, M., & Sunbul, M. R. (2018). Multiple approaches to assess human health risks from carcinogenic and non-carcinogenic metals via consumption of five fish species from a large reservoir in Turkey. Science of the Total Environment, 633, 684–694. Scholar
  67. Velusamy, A., Satheesh Kumar, P., Ram, A., & Chinnadurai, S. (2014). Bioaccumulation of heavy metals in commercially important marine fishes from Mumbai Harbor, India. Marine Pollution Bulletin, 81(1), 218–224. Scholar
  68. Verhaert, V., Newmark, N., D’Hollander, W., Covaci, A., Vlok, W., Wepener, V., et al. (2017). Persistent organic pollutants in the Olifants River Basin, South Africa: Bioaccumulation and trophic transfer through a subtropical aquatic food web. Science of the Total Environment, 586, 792–806. Scholar
  69. Walters, D., Jardine, T., Cade, B. S., Kidd, K., Muir, D., Leipzig-Scott, P., et al. (2016). Trophic magnification of organic chemicals: A global synthesis. Environmental Science & Technology, 50(9), 4650–4658.CrossRefGoogle Scholar
  70. Wang, H., Li, Y., Xia, X., & Xiong, X. (2018). Relationship between metabolic enzyme activities and bioaccumulation kinetics of PAHs in zebrafish (Danio rerio). Journal of Environmental Sciences (China), 65, 43–52. Scholar
  71. Wassenberg, T., & Hill, B. J. (1987). Natural diet of the tiger prawns Penaeus esculentus and P. semisulcatus. Marine and Freshwater Research, 38(1), 169–182.CrossRefGoogle Scholar
  72. Webster, L., Russell, M., Shepherd, N., Packer, G., Dalgarno, E. J., & Neat, F. (2018). Monitoring of Polycyclic Aromatic Hydrocarbons (PAHs) in Scottish Deepwater environments. Marine Pollution Bulletin, 128, 456–459. Scholar
  73. Won, E.-J., Choi, B., Hong, S., Khim, J. S., & Shin, K.-H. (2018). Importance of accurate trophic level determination by nitrogen isotope of amino acids for trophic magnification studies: A review. Environmental Pollution, 238, 677–690.CrossRefGoogle Scholar
  74. Yakan, S. D., Focks, A., Klasmeier, J., & Okay, O. S. (2017). Numerical evaluation of bioaccumulation and depuration kinetics of PAHs in Mytilus galloprovincialis. Environmental Pollution, 220(Pt B), 1244–1250. Scholar
  75. Yi, Y. J., & Zhang, S. H. (2012). The relationships between fish heavy metal concentrations and fish size in the upper and middle reach of Yangtze River. Procedia Environmental Sciences, 13, 1699–1707. Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Earth Sciences, College of ScienceShiraz UniversityShirazIran

Personalised recommendations