Skip to main content

Liver Concentrations of Copper, Zinc, Iron and Molybdenum in Sheep and Goats from Northern Greece, Determined by Energy-Dispersive X-Ray Fluorescence Spectrometry

Abstract

Energy-dispersive X-Ray fluorescence spectrometry was used to determine the concentrations of copper (Cu), zinc, iron and molybdenum in the liver of 76 sheep and goats from the regions of Macedonia-Thrace, northern Greece. In general, metal concentrations were in the adequate range, with one main exception of Cu-deficiency observed in all of the examined goat liver samples and Cu-toxicity found in 4 % of the sheep liver samples. One-way analysis of variance was carried out to determine significant differences among means depending on animal species, sex and age. Pearson correlation analysis was used to explore correlations between metal concentrations. The results obtained in the present study are discussed in the framework of diagnostic ranges, suggested for classifying the metal status of sheep and goats, and are compared with liver metal concentrations reported world-wide.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Adei E, Forson-Adaboh K (2008) Toxic (Pb, Cd, Hg) and essential (Fe, Cu, Zn, Mn) metal content of liver tissue of some domestic and bush animals in Ghana. Food Addit Contam: Part B 1:100–105

    CAS  Article  Google Scholar 

  2. Anke M, Seifert M (2007) The biological and toxicological importance of molybdenum in the environment and in the nutrition of plants, animals and man- part 1: molybdenum in plants. Acta Biol Hung 58:311–324

    CAS  Article  Google Scholar 

  3. Anke M, Seifert M, Holzinger S, Müller R, Schäfer U (2007) The biological and toxicological importance of molybdenum in the environment and in the nutrition of plants, animals and man- part 2: molybdenum in animals and man. Acta Biol Hung 58:325–333

    CAS  Article  Google Scholar 

  4. Anonymous (1999) Molybdenum. Canadian Water Quality Guidelines for the Protection of Aquatic Life, Canadian Council of Ministers of the Envirionment

    Google Scholar 

  5. Anonymous (2014) Contaminants found in groundwater, USGS water science school. http://water.usgs.gov/edu/groundwater-contaminants.html (downloaded on12/29/2014 at 10:39 PM)

  6. Anonymous (2014) Overview of molybdenum poisoning. The merck veterinary manual. www.merckmanuasls.com/vet/toxicology/molybdenum_poisoning/overview_of_molybdenum.poisoning.html

  7. Anonynous (1998) Zinc. Guidelines for interpretation of the biological effects of selected constituents in biota, water and sediment. National Irrigation Water Quality Program—Information Report No.3. US Department of Interior

  8. Antoniou V, Tsoukali H, Epivatianos P, Nathanael B (1989) Cadmium concentrations in beef consumable tissues in relation with age of animals and area of breeding. Bull Environ Contam Toxicol 43:915–919

    CAS  Article  Google Scholar 

  9. Benemariya H, Robberecht H, Deelstra H (1993) Zinc, copper, and selenium in milk and organs of cow and goat from Burundi, Africa. Sci Total Environ 128:83–98

    CAS  Article  Google Scholar 

  10. Blanco-Penedo I, Cruz JM, López-Alonso M, Miranda M, Castillo M, Hernández J, Benedito JL (2006) Influence of copper status on the accumulation of toxic and essential metals in cattle. Environ Int 32:901–906

    CAS  Article  Google Scholar 

  11. Blood DC, Radostits OM (1989) Veterinary medicine. A textbook of the diseases of Cattle, Sheep, Pigs, Goats and Horses, 7th edn. Baillière-Tindall, London

    Google Scholar 

  12. Bügel S (2003) Can human micronutrient status be improved by supplementing domestic animals? Proc Nutr Soc 62:399–402

    Article  Google Scholar 

  13. Christodoulopoulos G, Roubies N (2007) Diagnosis and treatment of copper poisoning caused by accindental feeding on poultry litter in a sheep flock. Aust Vet J 85:451–453

    CAS  Article  Google Scholar 

  14. Davis GK, Mertz W (1987) Copper. In: Mertz W (ed) Trace elements in human and animal nutrition, vol I. Academic Press, New York, pp 301–364

    Chapter  Google Scholar 

  15. De Sousa IKF, Minervino AHH, Sousa RS, Chaves DF, Soares HS, Barros IO, de Araújo CASC, Júnior RAB, Ortolani EL (2012) Copper deficiency in sheep with high liver iron accumulation. Vet Med Int. doi:10.1155/2012/207950

    Google Scholar 

  16. Doyle JJ (1977) Effects of low levels of dietary cadmium in animals: a review. J Environ Qual 6:111–116

    CAS  Article  Google Scholar 

  17. Eisler R (1993) Zinc hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish Wildl Serv Biolo Rep 26(10):106

    Google Scholar 

  18. Ellen G, van Loon JW, Tolsma K (1989) Copper, chromium, manganese, nickel and zinc in kidneys of cattle, pigs and sheep and in chicken livers in The Netherlands. Z Lebensm Unters For 189:534–537

    CAS  Article  Google Scholar 

  19. EPA (1980) Ambient water quality criteria for zinc. U.S. Environmental Protection Agency Report 44015-80-079, p.158

  20. EPA (1991) Water quality criteria summary. U.S. environmental protection agency, office of science and technology, health and ecological criteria division, Washington, DC

  21. EPA (1992) Water quality standards: establishment of numeric criteria for priority toxic pollutants; States’ compliance, final rule. Fed Reg 57:60910–60917

    Google Scholar 

  22. Evangelou C, Yiakoulaki M, Papanastasis V (2014) Spatio-temporal analysis of sheep and goats grazing in different forage resources of Northern Greece. Hacquetia 13:205–213

    Article  Google Scholar 

  23. Falandysz J (1991) Manganese, copper, zinc, iron, cadmium, mercury and lead in muscle meat, liver and kidneys of poultry, rabbit and sheep slaughtered in the northern part of Poland, 1987. Food Addit Contam 8:71–83

    CAS  Article  Google Scholar 

  24. Frøslie A, Norheim G, Rambæk JP, Steinnes E (1985) Heavy Metals in Lamb Liver: contribution from Atmospheric Fallout. Bull Environ Contam Toxicol 34:175–182

    Article  Google Scholar 

  25. Giannenas I, Leonidis G, Christofi A, Rossios K (2008) Overview of the situation of sheep production in the area of Eordea Kozani. J Hell Vet Med Soc 59:247–260

    Google Scholar 

  26. Gooneratne SR, Buckley WT, Christensen DA (1989) Review of copper deficiency and metabolism in ruminants. Can J Anim Sci 69:819–845

  27. Gurzau ES, Neagu C, Gurzau AE (2003) Essential metals—case study on iron. Ecotoxicol Environ Saf 56:190–200

    CAS  Article  Google Scholar 

  28. Hadjigeorgiou I (2011) Past, present and future of pastoralism in Greece. Pastoralism: research, policy and Practice 1: 24. doi:10.1186/2041-7136-1-24

  29. Hadjigeorgiou I, Vallerand F, Tsimpoukas K, Zervas G (1998) The socio-economics of sheep and goat farming in Greece, and the implications for future rural development. LSIRD BRAY CONFERENCE. http://www.macaulay.ac.uk/livestocksystems/dublin/hadgi.pdf. Accessed 14 Oct 2013

  30. Hellenic Statistical Authority [ELSTAT] (2010) Agriculture statistics of Greece, year 2006

  31. Herroux LL, Le Roux S, Appriou P, Martinez J (1997) Behaviour of metals following intensive pig slurry applications to a natural field treatment process in Britanny (France). Environ Pollut 97:119–130

    Article  Google Scholar 

  32. HMRF (2007) Hellenic Ministry of Rural Development and Food. Sheep and Goat sector Development (in greek). http://www.minagric.gr/images/stories/docs/ypoyrgeio/dimosieyseis-Arthra/meleti_gia_Nea_KAP/filadia_zoikis/aigoproboatotrofias.pdf. Accessed 27 Sept 2013

  33. Hoff B, Boermans HJ, Baird JD (1998) Retrospective study of toxic metal analyses requested at a veterinary diagnostic toxicology laboratory in Ontario (1990–1995). Can Vet J 39:39–43

    CAS  Google Scholar 

  34. Jordâo CP, Pereira MG, Bellato CR, Pereira JL, Matos AT (2002) Assessment of water systems for contaminants from domestic and industrial sewages. Environ Monit Assess 79:75–100

    Article  Google Scholar 

  35. Jorhem L, Sundström B, Astrand C, Haegglund G (1989) The levels of zinc, copper, manganese, selenium, chromium, nickel, cobalt and aluminium in the meat, liver and kidney of Swedish pigs and cattle. Z Lebensm Unters For 188:39–44

    CAS  Article  Google Scholar 

  36. Kincaid RL, Miller WJ, Fowler PR, Gentry RP, Hampton DL, Neathery MW (1976) Effect of high dietary zinc metabolism and intracellular distribution in cows and calves. J Dairy Sci 59:1580–1584

    CAS  Article  Google Scholar 

  37. Knowles SO, Grace ND (2014) A recent assessment of the elemental composition of New Zealand pastures in relation to meeting the dietary requirements of grazing livestock. J Anim Sci 92:303–310

    CAS  Article  Google Scholar 

  38. Lengarite MI, Mbugua PN, Gachuiri CK, Kabuage LW (2012) Mineral status of sheep and goats grazing in the arid rangelands of Northern Kenya. Pak J Nutr 11:383–390

    CAS  Article  Google Scholar 

  39. López Alonso M, Benedito UJL, Miranda M, Castillo C, Hernández J, Shore RF (2000a) Arsenic, cadmium, lead, copper and zinc in cattle from Galicia, NW Spain. Sci Total Environ 246:237–248

    Article  Google Scholar 

  40. López Alonso M, Benedito JL, Miranda M, Castillo C, Hernández J, Shore RF (2000b) The effect of pig farming on copper and zinc accumulation in cattle in Galicia (North-western Spain). Vet J 160:259–266

    Article  Google Scholar 

  41. Marques AVS, Soares PC, Riet-Correa F, Mota IO, Silva TLA, Borba Neto AV, Soares FAP, Alencar SP (2011) Serum and liver concentrations of copper, iron, zinc and molybdenum in sheep and goats in the state of Pernambuco. Pesquisa Vet Brasil 31:398–406

    Google Scholar 

  42. Menzies PI, Boermans H, Hoff B, Durzi T, Langs L (2003) Survey of the status of copper interacting minerals, and vitamin E levels in the livers of sheep in Ontario. Can Vet J 44:898–906

    CAS  Google Scholar 

  43. Mills CF (1974) The detection of trace element deficiency and excess in man and farm animals. Proc Nutr Soc 33:267–274

    CAS  Article  Google Scholar 

  44. Mills CF, Dalgarno AC (1972) Copper and zinc status of ewes and lambs receiving increased dietary concentrations of cadmium. Nature 239:171–173

    CAS  Article  Google Scholar 

  45. Nielsen FH (2012) History of zinc in agriculture. Adv Nutr 3:783–789

    CAS  Article  Google Scholar 

  46. Ortolani EL, Antonelli AC, de Souza Sarkis JE (2004) Acute copper poisoning from a copper sulphate footbath. Vet Hum Toxicol 45:289–293

    Google Scholar 

  47. Ott EA, Smith WH, Harrington RB, Beeson WM (1966) Zinc toxicity in ruminants. III. Physiological changes in tissues and alterations in rumen metabolism in lambs. J Anim Sci 25:424–431

    CAS  Google Scholar 

  48. Page AL, Chang AC, Adriano DC (1990) Deficiencies and toxicities of trace elements. Am Soc Civ Eng Man Rep Eng Pract 71:138–160

    Google Scholar 

  49. Park YW (1988) Trace mineral contents and Fe/Zn ratio in goat meat. J Food Comp Anal 1:283–289

    CAS  Article  Google Scholar 

  50. Polyzos N (1991) Utilization of rangelands (present situation, problems and prospective). Anim Sci Rev 22:25–35

  51. Pitt M, Fraser J, Thurley DC (1980) Molybnedum toxicity in sheep: epiphysiolysis, exotoses and biochemical changes. J Comp Pathol 90:567–576

    CAS  Article  Google Scholar 

  52. Puls R (1994) Mineral levels in animal health. Sherpa International, Canada

    Google Scholar 

  53. Radostits OM, Gay CC, Blood Dc, Hinchcliff KE (Eds) (2000) Primary copper poisoning. In Veterinary Medicine, 9th edn. WB Saunders, London, UK, pp 1599–1603

  54. Reykdal Ó, Thorlacius A (2001) Cadmium, mercury, iron, copper, manganese and zinc in the liver and kidney of the Icelandic lamb. Food Addit Contam 18:960–969

    CAS  Article  Google Scholar 

  55. Roubies N, Giadinis ND, Polizopoulou Z, Argiroudis S (2008) A retrospective study of chronic copper poisoning in 79 sheep flocks in Greece (1987–2007). J Vet Pharmacol Ther 31:181–183

    CAS  Article  Google Scholar 

  56. Saylor WW, Leach RM Jr (1980) Intracellular distribution of copper and zinc in sheep: effect of age and dietary levels of the metals. J Nutr 110:448–459

    CAS  Google Scholar 

  57. Schwan O, Jacobsson S-O, Frank A, Rudby-Martin L, Petersson LR (1987) Cobalt and copper deficiency in Swedish landrace pelt sheep: application of diagnostics in flock-related deficiency diseases. J Vet Med A 34:709–718

    CAS  Article  Google Scholar 

  58. Scott PR (2007) Copper toxicity. Sheep medicine. Manson Publishing, London, pp 293–295

    Google Scholar 

  59. Smith OB, Akinbamijo OO (2000) Micronutrients and reproduction in farm animals. Anim Reprod Sci 60–61:549–560

    Article  Google Scholar 

  60. Soetan KO, Olaiya CO, Oyewole OE (2010) The importance of mineral elements for humans, domestic animals and plants: a review. Afr J Food Sci 4:200–222

    CAS  Google Scholar 

  61. Sommerville GF, Mason JB (1978) Copper overdosage in sheep. N Z Vet J 33:98–99

    Article  Google Scholar 

  62. Spolders M, Höltershinken M, Rehage J, Flachowsky G (2011) Trace element supply of cattle in the area of conflich between sufficient supply of the animals and interests of consumer and environmental protection. Prakt Tierarzt 92:998–1008

    Google Scholar 

  63. Standish JF, Ammerman CB, Palmer AZ, Simpson CF (1971) Influence of dietary iron and phosphorus on performance, tissue mineral composition and mineral absorption in steers. J Anim Sci 33:171–178

    CAS  Google Scholar 

  64. Steinnes E (2009) Soils and geomedicine. Environ Geochem Health 31:523–535

    CAS  Article  Google Scholar 

  65. Suttle NF (2010) Mineral nutrition of livestock. CAB International, Wallingford

    Book  Google Scholar 

  66. Swaileh KM, Abdulkhaliq A, Hussein RM, Matani M (2009) Distribution of toxic metals in organs of local cattle, sheep, goat and poultry from the West Bank, Palestinian authority. Bull Environ Contam Toxicol 83:265–268

    CAS  Article  Google Scholar 

  67. Underwood EJ (1959) Trace elements in human and animal nutrition, 2 Printing edn. Academic Press Inc, New York

    Google Scholar 

  68. Underwood EJ, Suttle NF (1999) The mineral nutrition of livestock, 3rd edn. CAB International, Wallingford

    Book  Google Scholar 

  69. Wolkers H, Wensing T, Groot Bruinderink GWTA (1994) Heavy metal contamination in organs of red deer (Cervus elaphus) and wild boar (Sus scrofa) and the effect on some trace elements. Sci Total Environ 144:191–199

    CAS  Article  Google Scholar 

  70. Xing W, Liu G (2011) Iron biochemistry and its environmental impacts in freshwater lakes. Fresen Environ Bull 20:1339–1345

    CAS  Google Scholar 

  71. Xylouri-Frangiadaki E, Papadopoulou C, Bryoni E (2002) Can zinc be used to the treatment of Microsporum gypseum dermatitis in man as well in sheep? Int J Antimicrob Agent 20:230–231

    CAS  Article  Google Scholar 

  72. Zantopoulos N, Antoniou V, Petsaga V, Zdragas A (1995) Copper concentrations in sheep liver and kidney in Greece. Vet Hum Toxicol 38:184–185

    Google Scholar 

  73. Zantopoulos N, Antoniou V, Nikolaidis E (1999) Copper, zinc, cadmium, and lead in sheep grazing in North Greece. Bull Environ Contam Toxicol 62:691–699

    CAS  Article  Google Scholar 

  74. Zervas G, Nikolaou E, Mantzios A (1990) Comparative study of chronic copper poisoning in lambs and young goats. Anim Prod 50:497–506

    CAS  Article  Google Scholar 

Download references

Acknowledgments

Measurements were carried out at the energy-dispersive XRF spectrometry unit of the University of Ioannina.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Christina Papachristodoulou.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Papachristodoulou, C., Stamoulis, K., Tsakos, P. et al. Liver Concentrations of Copper, Zinc, Iron and Molybdenum in Sheep and Goats from Northern Greece, Determined by Energy-Dispersive X-Ray Fluorescence Spectrometry. Bull Environ Contam Toxicol 94, 460–467 (2015). https://doi.org/10.1007/s00128-015-1496-6

Download citation

Keywords

  • Heavy metals
  • Liver
  • Sheep
  • Goat
  • Greece
  • EDXRF spectrometry