Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

A study on the concentration of heavy metals and histopathological changes in Persian jirds (Mammals; Rodentia), affected by mining activities in an iron ore mine in Iran

  • 158 Accesses

  • 1 Citations

Abstract

Mining activity constitutes a potential source of heavy metal pollution in the environment. Long-term exposure to heavy metals (e.g., cadmium) has adverse health effects. Rodents frequently serve as bioindicators to monitor the levels of heavy metals in the environment. In the present study, concentrations of 10 heavy metals (Cd, Co, Cr, Cu, Fe, Mo, Ni, Pb, Sb, and Zn) in kidney, liver, and muscle tissue of the Persian jird (Meriones persicus) were evaluated. This is the first study to examine the histopathological changes in Persian jird tissues caused by the bioaccumulation heavy metals. The samples were taken at location that surrounded by Sangan Iron Ore Mine (SIOM) mining activities, in northeastern Iran. The results show that the highest concentrations for the metals were observed in kidney and liver, whereas lowest concentrations were found in muscle of Persian jirds. The concentration of Pb was below the limit of detection. Sex and age were two factors that could explain the different levels of heavy metal bioaccumulation, which affects the concentration of some metals. Adults had significantly higher Cu and Cd levels compared to juveniles. Males bioaccumulated more Zn in their kidneys than females, whereas females bioaccumulated more Fe in their livers. As expected, heavy metals affected various organs of the studied specimens. Hyperemia, hemorrhage, necrosis, and degenerative damage to the epithelial cells of the tubules, the presence of hyaline casts, and in one case, mononuclear leukocyte infiltration, were observed in samples of renal tissue. Hemorrhage and hepatocyte vacuolization were the most common histopathological changes found in samples of hepatic tissue. These effects and the concentrations of heavy metals in the studied specimens indicate the need for monitoring and frequent sampling to evaluate long-term persistent pollutants.

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

Fig. 1
Fig. 2

References

  1. Agency for Toxic Substances and Disease Registry (ATSDR) (2015). Toxicological Profile for Molybdenum. Available at <https://www.atsdr.cdc.gov/toxprofiles/TP.asp?id=1482&tid=289>; [Accessed on 12. 09. 2017]

  2. Agency for Toxic Substances and Disease Registry (ATSDR) (1997) Toxicological profile for nickel (update), Public health service, U.S. Department of Health and Human Services, Atlanta, GA

  3. Alonso ML, Benedito JL, Miranda M, Castillo C, Hernández J, Shore RF (2002) Interactions between toxic and essential trace metals in cattle from a region with low levels of pollution. Arch Environ Contam Toxicol 42:165–172

  4. Bancroft JD, Stevens A (1996) Theory and practice of histological techniques, 4th edn. Churchill Livingstone, New York

  5. Barrett HM, Irwin DA, Semmons E (1947) Studies on the toxicity of inhaled cadmium The acute toxicity of cadmium oxide by inhalation. J Ind Hyg Toxicol 29:279–285

  6. Betty J, Leavitt R, Biondo N, Polin D (1990) An ecotoxicological study of a population of white-footed mouse inhabiting a polychlorinated biphenyls-contaminated area. Arch Environ Contam Toxicol 19:283–290

  7. Beardsley A, Vagg MJ, Beckett PHT, Sansom BF (1978) Use of the field vole (M. Agrestis) for monitoring potentially harmful elements in the environment. Environ Pollut 16:65–71

  8. Beernaert J, Schiers J, Leirs H, Blust R, Van Hagen R (2007) Nondestructive pollution exposure assessment by means of wood mice hair. Environ Pollut 145:443–451

  9. Bellés M, Albina ML, Sánchez DJ, Corbella J, Domingo JL (2002) Interactions in developmental toxicology: effects of concurrent exposure to lead, organic mercury, and arsenic in pregnant mice. Arch Environ Contam Toxicol 42:93–98

  10. Bernard A (2008) Cadmium & its adverse effects on human health. Indian J Med Res 4:557–564

  11. Bonilla-Valverde D, Ruiz-Laguna J, Muñoz A, Ballesteros J, Lorenzo F, Gómez-Ariza JL, López-Barea J (2004) Evolution of biological effects of Aznalcólla mining spill in the Algerian mouse (Mus spretus) using biochemical biomarkers. Toxicology 197:123–138

  12. Bragadin M, Toninello A, Bindoli A, Rigobello MP, Canton M (2003) Thallium induces apoptosis in Jurkat cells. Ann N Y Acad Sci 1010:283–291

  13. Brzóska M, Jakoniuk JM, Marcinkiewicz BP, Sawicki B (2003) Liver and kidney function and histology in rats exposed to cadmium and ethanol. Alcohol Alcohol 38(1):2–10. https://doi.org/10.1093/alcalc/agg006

  14. Chaworth-Musters JL, Ellerman JR (1947) A revision of the genus Meriones. Proceeding zoology. Soc Lond 117(2–3):478–504

  15. Christopher WD (1986) Mammals as biological monitors of environmental metal levels. Environ Monit Assess 6:127–144

  16. Clark DR, Foerster KS, Marn CM, Hothem RL (1992) Uptake and environmental contaminants by small mammals in pickleweed habitats at San Francisco Bay, California. Arch Environ Contam Toxicol 22:389–396

  17. Cooke J, Andrews S, Johnson M (1990) The accumulation of lead, zinc, cadmium, and fluoride in the wood mouse (Apodemus sylvaticus L.). Water Air Soil Pollut 51:55–63

  18. Dabiri R, Bakhshi-Mazdeh M, Mollai H (2017) Heavy metal pollution and identification of their sources in soil over Sangan iron-mining region, NE Iran. Journal of mining & Environment 8(2)277–289. https://doi.org/10.22044/jme.2016.820

  19. Damek-Poprawa M, Sawicka-Kapusta K (2003) Damage to the liver, kidney, and testis with reference to burden of heavy metals in yellow-necked mice from areas around steelworks and zinc smelters in Poland. Toxicology 186:1–10

  20. Damek-Poprawa M, Sawicka-Kapusta K (2004) Histopathological changes in the liver, kidneys, and testes of bank voles environmentally exposed to heavy metal emissions from the steelworks and zinc smelter in Poland. Environ Res 96:72–78

  21. Darvish J (2011) Morphological comparison of fourteen species of the genus Meriones Illiger, 1811 (Gerbillinae, Rodentia), from Asia and North Africa. Iran J Anim Biosyst (IJAB) 7(1):49–74

  22. Faroon O, Ashizawa A, Wright S, Tucker P, Jenkins K (2012) Toxicological profile for cadmium. Agency for Toxic Substances and Disease Registry (ATSDR). Division of toxicology and human health sciences (proposed). Atlanta, GA, p 487

  23. Firouz S (2005) The complete Fauna of Iran. London: I. B. Tauris Press, p 322

  24. Friberg L (1950) Health hazards in the manufacture of alkaline accumulators with special reference to chronic cadmium poisoning. Acta Medica Scandinavica 240:1–124

  25. Furness RW, Greenwood JJD, Jarvis PJ, Lehr Brisbin I, Ormerod SJ, Tyler SJ, Montevecchi WA, Baillie SR, Crick HQP, Marchant JH, Peach WJ (1993) Birds as monitors of environmental changes. Chapman and Hall, Cornwall

  26. García-Sevillano MA, García-Barrera T, Navarro F, Abril N, Pueyo C, López-Barea J, Gómez-Ariza JL (2014) Use of Metallomics and metabolomics to assess metal pollution in Doñana National Park (SW Spain). Environ Sci Technol: Environmental Science & Technology 48:7747–7755. https://doi.org/10.1021/es4057938

  27. Goyer A (1991) Toxic effects of metals. In: Amdur MO, Doull JD, Klaassen CD (eds) Casarett and Doull's toxicology, 4thed edn. Pergamon Press, New York, pp 623–680

  28. Goyer RA (1997) Toxic and essential metal interactions. Annu Rev Nutr 17:37–50

  29. Gonzalez XI, Aboal JR, Fer_nandez JA, Carballeira A (2008) Evaluation of some sources of variability in using small mammals as pollution biomonitors. Chemosphere 71:2060–2067

  30. Gumbleton M, Nicholls PJ (1988) Dose-response and time-response biochemical and histological study of potassium dichromate-induced nephrotoxicity in the rat. Food Chem Toxicol 26:37–44

  31. Haschek WM, Rousseaux CG (1998) Fundamentals of Toxicologic pathology. Academic Press, San Diego, p 563

  32. Hunter BA, Johnson MS, Thompson DJ (1989) Ecotoxicology of copper and cadmium in contaminated grassland ecosystem III Small mammals. J Appl Ecol 26:89–99

  33. Jadhav SH, Sarkar SN, Patil RD, Tripathi HC (2007) Effects of subchronic exposure via drinking water to a mixture of eight water-contaminating metals: a biochemical and histopathological study in male rats. Arch Environ Contam Toxicol 53:667–677

  34. Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72. https://doi.org/10.2478/intox-2014-0009

  35. Järup L, Berglund M, Elinder CG, Nordberg G, Vahter M (1998) Health effects of cadmium exposure - a review of the literature and a risk estimate. Scand J Work Environ Health 24:1–51

  36. Khazaee M, Hamidian AH, Alizadeh-Shabani A, Ashrafi S, Mirjalili SAA, Esmaeilzadeh E (2015) Accumulation of heavy metals and as in liver, hair, femur, and lung of Persian jird (Meriones persicus) in Darreh Zereshk copper mine, Iran. Environ Sci Pollut Res 23:3860–3870. https://doi.org/10.1007/s11356-015-5455-x

  37. Kojadinovic J, Potier M, Le Corre M, Cosson R, Bustamante P (2007) Bioaccumulation of trace elements in pelagic fish from the Western Indian Ocean. Environ Pollut 146:548–566

  38. Komarnicki GJK (2000) Tissue, sex and age-specific accumulation of heavy metals (Zn, cu, Pb, cd) by populations of the mole (Talpa europaea L.) in a central urban area. Chemosphere 41:1593–1602

  39. Kong L, Tang M, Zhang T, Wang D, Hu K, Lu W, Wei C, Liang G, Pu Y (2014) Nickel nanoparticles exposure and reproductive toxicity in healthy adult rats. Int J Mol Sci 15:21253–21269. https://doi.org/10.3390/ijms151121253

  40. Kraus U, Wiegand J (2006) Long-term effects of the Aznalcóllar mine spill-heavy metal content and mobility in soils and sediments of the Guadiamar river valley (SW Spain). Sci Total Environ 36:7855–7871

  41. Leita L, Enne G, De Nobili M, Baldini M, Sequi P (1991) Heavy metal bioaccumulation in lamb and sheep bred in smelting and mining areas of S.W. Sardinia (Italy). Bull Environ Contam Toxicol 46:887–893

  42. Leonard SS, Harris GK, Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Radic Biol Med 37:1921–1942

  43. Ma WC, Denneman W, Faber J (1991) Hazardous exposure of ground-living small mammals to cadmium and lead in contaminated terrestrial ecosystems. Arch Environ Contam Toxicol 20:266–270

  44. Mar’quez-Ferrando R, Santos X, Pleguezuelos JM, Ontiveros D (2009) Bioaccumulation of heavy metals in the lizard Psammodromus algirus after a tailing-dam collapse in Aznalco’llar (Southwest Spain). Arch Environ Contam Toxicol 56:276–285. https://doi.org/10.1007/s00244-008-9189-3

  45. Marques CC, Sánchez-Chardi A, Gabriel SI, Nadal J, Viegas-Crespo AM, Mathias ML (2007) How does the greater white-toothed shrew, Crocidura russula, responds to long-term heavy metal contamination? - a case study. Sci Total Environ 376:128–133

  46. Mažeikytė R, Balčiauskas L (2003) Heavy metal concentrations in bank voles (Clethrionomys glareolus) from protected and agricultural territories of Lithuania. Acta Zoologica Lituanica 13:48–60

  47. McLean CM, Koller CE, Rodger JC, MacFarlane GR (2009) Mammalian hair as an accumulative bioindicator of metal bioavailability in Australian terrestrial environments. Sci Total Environ 407:3588–3596

  48. Millán J, Mateo R, Taggart MA, López-Bao JV, Viota M, Monsalve V, Camarero PR, Blázquezc E, Jiménezc B (2008) Levels of heavy metals and metalloids in critically endangered Iberian lynx and other wild carnivores from Southern Spain. Sci Total Environ 399:193–201

  49. Milton AG, Zalewski PD, Ratnaike RN (2004) Zinc protects against Arsenic-induced Apoptosis. Biometals. Biometals 17(6):707–713. https://doi.org/10.1007/s10534-004-1210-3

  50. Mugford CA, Kedderis GL (1998) Sex-dependent metabolism of xenobiotics. Drug Metab Rev 30:441–498

  51. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8

  52. Nordberg G, Nogawa K, Nordberg M, Friberg L (2007) Cadmium. In: Nordberg G, Fowler B, Nordberg M, Friberg L (eds) Handbook on toxicology of metals. Academic Press, New York, pp 65–78

  53. Levengood J, Heske E (2008) Heavy metal exposure, reproductive activity and demographic patterns in white-footed mice (Peromyscus leucopus) inhabiting a contaminated floodplain wetland. Sci Total Environ 389:320–328

  54. Lopes PA, Viegas-Crespo AM, Nunes AC, Pinheiro T, Marques C, Santos MC, Mathias ML (2002) Influence of age, sex, and sexual activity on trace element levels and antioxidant enzyme activities in field mice (Apodemus sylvaticus and Mus spretus). Biol Trace Elem Res 85:227–239

  55. Pankakoski E, Hyvärinen H, Jalkanen M, Koivisto I (1993) Accumulation of heavy metals in the mole in Finland. Environ Pollut 80:9–16

  56. Pavlinov IY (2008) A review of phylogeny and classification of Gerbillinae (Mammalia :Rodentia). Moscow Univ. Publ, Moscow

  57. Pereira R, Pereira ML, Ribeiro R, Goncalves F (2006) Tissues and hair residues and histopathology in wild rats (Rattus rattus L.) and Algerian mice (Mus spretus Lataste) from an abandoned mine area (Southeast Portugal). Environ Pollut 139:561–575

  58. Pereira AA, Hattum B, Brouwer A, van Bodegom PM, Rezende CE, Salomons W (2008) Effects of iron-ore mining and processing on metal bioavailability in a tropical coastal lagoon. J Soils Sediments 8:239–252. https://doi.org/10.1007/s11368-008-0017-1

  59. Phelps K, McBee K (2008) Ecological characteristics of small mammal communities at a superfund site. Am Midl Nat 1:57–68

  60. Rainbow SP, Phillipsm DJH (1993) Cosmopolitan biomonitors of trace metals. Mar Pollut Bull 26:593–601. https://doi.org/10.1016/0025-326X(93)90497-8

  61. Rehman K, Fatima F, Waheed I, Akash MSH (2018) Prevalence of exposure of heavy metals and their impact on health consequences. J Cell Biochem 119:157–184

  62. Rogival D, Scheirs J, Blust R (2007) Transfer and accumulation of metals in a soil-diet-wood mouse food chain along a metal pollution gradient. Environ Pollut 145:516–528

  63. Quinn JA (2010) Trace metal concentrations across trophic levels in cotton fields of Xinjiang Province. MSc Thesis, B.S., Governors State University, China

  64. Salamat N, Etemadi-Deylami E, Movahedini A, Mohammadi Y (2014) Heavy metals in selected tissues and histopathological changes in liver and kidney of common moorhen (Gallinula chloropus) from Anzali wetland, the South Caspian Sea, Iran. Ecotoxicol Environ Saf 110:298–307

  65. Sánchez-Chardi A, Marques CC, Nadal J, Mathias ML (2007a) Metal bioaccumulation in the greater white-toothed shrew, Crocidura russula, inhabiting an abandoned pyrite mine site. Chemosphere 67:121–130

  66. Sánchez-Chardi A, López-Fuster MJ, Nadal J (2007b) Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): sex- and age-dependent variation. Environ Pollut 145:7–14

  67. Sánchez-Chardi A, Nadal J (2007) Bioaccumulation of metals and effects of a landfill in small mammals. Part I. The greater white-toothed shrew, Crocidura russula. Chemosphere 68:703–711

  68. Sánchez-Chardi A, Penarroja-Matutano C, Oliveira-Ribeiro CA, Nadal J (2007c) Bioaccumulation of metals and effects of a landfill in small mammals. Part II. The wood mouse, Apodemus sylvaticus. Chemosphere 70:101–110

  69. Sánchez-Chardi A, Oliveira-Ribeiro C, Nadal J (2009) Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana. Chemosphere 76:387–394

  70. Schleich CE, Beltrame MO, Antenucci CD (2010) Heavy metals accumulation in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae) from areas with different risk of contamination. Folia Zool 59:108–114

  71. Selim HM, Sparks DL (2001) Heavy metals release in soils. CRC Press/Lewis publisher, Boca Raton, p 264

  72. Sengupta P (2013) The laboratory rat: relating its age with humans. Int J Prev Med 6:624–630

  73. Shahsavari A, Akbari M (2018) Potential of solar energy in developing countries for reducing energy-related emissions. Renew Sust Energ Rev 90:275–291

  74. Shore RF, Douben PET (1994) The ecotoxicological significance of cadmium intake and residues in terrestrial small mammals. Ecotoxicol Environ Saf 29:101–112

  75. Storelli MM, Storelli A, D’Addabbo R, Marano C, Bruno R, Marcotrigiano GO (2005) Trace elements in loggerhead turtles (Caretta caretta) from the eastern Mediterranean Sea: overview and evaluation. Environ Pollut 135:163–170

  76. Sumbera R, Burda H, Chitaukali W N, Gannon W (2003) Reproductive biology of a solitary subterranean bathyergid rodent, the silvery mole-rat (Heliophobius argenteocinereus). J Mammal 84(1):278–287. https://doi.org/10.1644/1545-1542(2003)084<0278:RBOASS>2.0.CO;2

  77. S’wiergosz-Kowalewska R (2001) Cadmium distribution and toxicity in tissues of small rodents. Microsc Res Tech 55:208–222

  78. Świergosz-Kowalewska R, Gramatyka M, Reczyński W (2005) Metals distribution and interactions in tissues of shrews (Sorex spp.) from copper- and zinc-contaminated areas in Poland. J Environ Qual 34:1519–1529

  79. Szyczewski P, Siepak J, Niedzielski P, Sobczyński T (2009) Research on heavy metals in Poland. Pol J Environ Stud 18:755–768

  80. Orlowski C, Piotrowski JK (2003) Biological levels of cadmium and zinc in the small intestine of non-occupationally exposed human subjects. Hum Exp Toxicol 22:57–63

  81. Okati N, Rezaee M (2013) Heavy metals concentrations in different tissues of Persian Jird (Meriones persicus) in Sistan region. International Research Journal of Applied and Basic Sciences 10:1272–1276

  82. Tabatabaei Yazdi F, Adriaens D (2011) Patterns of phenotypic skull variation in M. persicus (Rodentia: Muridae) in relation to geoclimatical conditions. Iranian Journal of Animal Biosystematics (IJAB) 7(2):129–142

  83. Talmage SS, Walton BT (1991) Small mammals as monitors of environmental contaminants. Rev Environ Contam Toxicol 119:47–145

  84. Topolska K, Sawicka-Kapusta K, Cieslik E (2004) The effect of contamination of the Krakow region on heavy metals content in the organs of bank voles (Clethrionomys glareolus, Schreber, 1780). Pol J Environ Stud 13:103–109

  85. Tovar-Sánchez E, Cervantes LT, Martínez C, Rojas E, Valverde M, Ortiz-Hernández ML, Mussali-Galante P (2012) Comparison of two wild rodent species as sentinels of environmental contamination by mine tailings. Environ Sci Pollut Res 19:1677–1686

  86. Williams GM, Iatropoulos MJ (2002) Alteration of liver cell function and proliferation: differentiation between adaptation and toxicity. Toxicol Pathol 30:41–53

  87. Vahter M, Åkesson A, Lidén C, Ceccatelli S, Berglund M (2007) Gender differences in the disposition and toxicity of metals. Environ Res 104:85–95

  88. Viarengo A, Canesi L (1991) Mussels as biological indicators of pollution. Aquaculture 94:225–243

  89. Wester PW, van der Ven LTM, Vethaak AD, Grinwis GCM (2002) Aquatic toxicology: opportunities for enhancement through histopathology. Environ Toxicol Pharmacol 11:289–295

  90. Wintz H, Fox T, Vulpe C (2002) Responses of plants to iron, zinc and copper deficiencies. Biochem Soc Trans 30:766–768

  91. Wlostowski T, Krasowska A, Bonda E (2003) An iron-rich diet protects the liver and kidneys against cadmium-induced injury in the bank vole (Clethrionomys glareolus). Ecotoxicol Environ Saf 54:194–198

  92. Ware GW (2000). Reviews of environmental contamination and toxicology: continuation of residue reviews. Springer Science & Business Media. 146

  93. Zabowski D, Henry CL, Zheng Z, Zhang X (2001) Mining impacts on trace metal content of water, soil, and stream sediments in the Hei River basin, China. Water Air Soil Pollut 131:261–273

  94. Zarrintab M, Mirzaei R (2017) Evaluation of some factors influencing on variability in bioaccumulation of heavy metals in rodent’s species: Rombomys opimus and Rattus norvegicus from Central Iran. Chemosphere 169:194–203

  95. Ziaie H (2008) A field guide to the mammals of Iran. Iran wildlife Center, Tehran (In Persian)

Download references

Acknowledgments

The authors would like to thank the Iranian Department of Environment and the Sangan Iron Ore mine in Khaf, Iran, for their support of this research project. The authors also would like to thank the anonymous reviewers for their careful reading of our manuscript and helpful suggestions.

Funding

The project was funded by Ferdowsi University of Mashhad (#44692).

Author information

Correspondence to Fatemeh Tabatabaei Yazdi.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Philippe Garrigues

Electronic supplementary material

ESM 1

(DOCX 13 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shahsavari, A., Tabatabaei Yazdi, F., Moosavi, Z. et al. A study on the concentration of heavy metals and histopathological changes in Persian jirds (Mammals; Rodentia), affected by mining activities in an iron ore mine in Iran. Environ Sci Pollut Res 26, 12590–12604 (2019). https://doi.org/10.1007/s11356-019-04646-9

Download citation

Keywords

  • Iron ore mine
  • Pollution
  • Rodents
  • Heavy metals
  • Histopathology