Blood and hair as non-invasive trace element biological indicators in growing rabbits

George Papadomichelakis, Athanasios C Pappas, Evangelos Zoidis, Georgios Danezis, Konstantinos A Georgiou, Konstantinos Fegeros


The suitability of blood and hair as non-invasive tools to monitor trace element contents was studied in 48 Hyla male growing rabbits. Three diets with increasing organic selenium (Se) addition (0.1, 0.5 and 2.5 mg/kg) were used to induce alterations in the concentrations of trace elements vs. an unsupplemented diet. In blood, a linear decrease in Co (P<0.001), Cu (P<0.001), Mn (P<0.05), Zn (P<0.05), Sb (P<0.001), As (P<0.001), Cr (P<0.001), Mo (P<0.001), Ni (P<0.001) and Cd (P<0.001) concentrations with increasing dietary Se was observed. In hair, a cubic effect of dietary Se on Co (P<0.01), Cu (P<0.05), Mn (P<0.001), Pb (P<0.05), Mo (P<0.05) and Cd (P<0.05) concentrations was found, while As, Cr and Ni concentrations decreased linearly (P<0.01, P<0.01 and P<0.001, respectively) with increasing dietary Se. Selenium was negatively correlated to Sb, As, Cr, Mo, Ni and Cd, (P<0.001) in blood, and to As (P<0.05), Cr, Ni (P<0.01) and Pb (P<0.05) in hair. The contents of Se, As, Cr and Ni in blood were highly correlated (P<0.001) to those in hair. Blood appeared to be more sensitive than hair in detecting small changes in the trace element profile in rabbits, as was indicated by the discriminant analysis. In conclusion, blood and hair can be suitable biological indicators of essential, toxic and potentially toxic trace element status in rabbits, particularly when used complementarily.


biological indicators; blood; hair; organic selenium; rabbits; trace elements

Full Text:



Barbosa F.J., Tanus-Santos J.E., Gerlach R.F., Parsons P.J. 2005. A critical review of biomarkers used for monitoring human exposure to lead: advantages, limitations, and future needs. Environ. Health Persp., 113: 1669-1674.

Bryan C.E., Christopher S.J., Balmer B.C., Wells R.S. 2007. Establishing baseline levels of trace elements in blood and skin of bottlenose dolphins in Sarasota Bay, Florida: implications for non-invasive monitoring. Sci. Total Environ., 388: 325-342.

Čobanová K., Chrastinová Ľ., Chrenková M., Polačiková M., Formelová Z., Ivanišinová O., Ryzner M., Grešáková Ľ. 2018. The effect of different dietary zinc sources on mineral deposition and antioxidant indices in

rabbit tissues World Rabbit Sci., 26: 241-248.

de Blas C., Mateos G.G. 2010. Feed formulation. In ‘The Nutrition of the Rabbit (2nd ed.)’. C de Blas, J. Wiseman (Eds.) 222-231. CAB International: Wallingford, UK.

De Temmerman L., Vanongeval L., Boon W., Hoenig M., Geypens M. 2003. Heavy metal content of arable soils in northern Belgium. Water Air Soil Poll., 148: 61-76.

FEDNA (2003). Fundación Española para el Desarrollo de la Nutrición Animal. In C. De Blas, G. G. Mateos, & P. G. Rebollar (Eds.), Tablas FEDNA de composición y valor nutritivo de alimentos para la fabricación de piensos (2nd ed.). Madrid, Spain: FEDNA.

Georgiou C.A., Koupparis M.A. 1990. Automated flow injection spectrophotometric determination of para- and metasubstituted phenols of pharmaceutical interest based on their oxidative condensation with 1-nitroso-2-naphthol. Analyst, 115: 309-313.

Georgiou C.A., Danezis G.P. 2015. Elemental and isotopic mass spectrometry. In ‘Advanced Mass Spectrometry for Food, Comprehensive Analytical Chemistry’. (Ed. Y Pico) 131-243. Elsevier: Amsterdam.

Glynn A.W., Ilback N.G., Brabencova D., Carlsson L., Enqvist E.C., Netzel E., Oskarsson A. 1993. Influence of sodium selenite on 203Hg absorption, distribution and elimination in male mice exposed to methyl 203Hg. Biol. Trace Elem. Res., 39: 91-107.

Gulson B.L., Mizon K.J., Korsch M.J., Howarth D., Phillips A., Hall J. 1996. Impact on blood lead in children and adults following relocation from their source of exposure and contribution of skeletal tissue to blood lead. B. Environ. Contam. Tox., 56: 543-550.

Hasan M.Y., Kosanovic M., Fahim M.A., Adem A., Petroianu G. 2004. Trace metal profiles in hair samples from children in urban and rural region of the United Arab Emirates. Vet. Hum. Toxicol., 46: 119-121.

He K. 2011. Trace elements in nails as biomarkers in clinical research. Eur. J. Clin. Invest., 41: 98-102.

Käkelä R., Käkelä A., Hyvärinen H. 1999. Effects of nickel chloride on reproduction of the rat and possible antagonistic role of selenium. Comp. Biochem. Physiol. C, 123: 27-37.

Kan C.A., Meijer G.A.L. 2007. The risk of contamination of food with toxic substances present in animal feed. Anim. Feed Sci. Technol., 133: 84-108.

Keil D.E., Berger-Ritchie J., McMillin G.A. 2011. Testing for toxic elements: a focus on arsenic, cadmium, lead, and mercury. Labmedicine, 42: 735-742.

Klotz L.O., Kröncke K.D., Buchczyk D.P., Sies H. 2003. Role of copper, zinc, selenium and tellurium in the cellular defense against oxidative and nitrosative stress. J. Nutr., 133: 1448-1451.

Levander O.A. 1977. Metabolic interrelationships between arsenic and selenium. Environ. Health Persp., 19: 159-164.

López-Alonso M.L., Benedito J.L., Miranda M., Castillo C., Hernández J., Shore R.F. 2002. Cattle as biomonitors of soil arsenic, copper and zinc concentrations in Galicia (NW Spain). Arch. Environ. Contam. Toxicol., 43: 103-108.

McDowell L.R. 2003. ‘Minerals in animal and human nutrition (2nd ed)’. (Elsevier Science: Amsterdam).

Milošković A., Simić V. 2015. Arsenic and other trace elements in five edible fish species in relation to fish size and weight and potential health risks for human consumption. Pol. J. Environ. Stud., 24: 199-206.

Miranda M., López-Alonso M., Castillo C., Hernández J., Benedito J.L. 2005. Effects of moderate pollution on toxic and trace metal levels in calves from a polluted area of northern Spain. Environ. Int., 31: 543-548.

Ohta H., Seki Y., Yoshikawa H. 1995. Interactive effects of selenium on chronic cadmium toxicity in rats. ACES Bulletin, 8: 97-104. Othman A.I., El Missiry M.A. 1998. Role of selenium against lead toxicity in male rats. J. Biochem. Mol. Toxic., 12: 345-349.;2-V

Papadomichelakis G., Zoidis E., Pappas A.C., Mountzouris K.C., Fegeros K. 2017. Effects of increasing dietary organic selenium levels on meat fatty acid composition and oxidative stability in growing rabbits. Meat Sci., 131: 132-138.

Papadomichelakis G., Zoidis E., Pappas A.C., Danezis G., Georgiou C.A., Fegeros K. 2018. Dietary organic selenium addition and accumulation of toxic and essential trace elements in liver and meat of growing rabbits. Meat Sci., 145: 383-388.

Pappas A.C., Zoidis E., Georgiou C.A., Demiris N., Surai P.F., Fegeros K. 2011. Influence of organic selenium supplementation on the accumulation of toxic and essential trace elements involved in the antioxidant system

of chicken. Food Addit. Contam. Part A, 28: 446-454.

Park D.U., Kim D.S., Yu S.D., Lee K.M., Ryu S.H., Kim S.G. et al. 2014. Blood levels of cadmium and lead in residents near abandoned metal mine areas in Korea. Environ. Monit. Assess., 186: 5209-5220.

Patra R.C., Swarup D., Naresh R., Kumar P., Nandi D., Shekhar P., Roy S., Ali S.L. 2007. Tail hair as an indicator of environmental exposure of cows to lead and cadmium in different industrial areas. Ecotoxicol. Environ. Saf., 66: 127-131.

Paukert J., Obrusnik I. 1986. The hair of the common hare (Lepus europaeus Pall.) and of the common vole (Microtus arvalis Pall.) as indicator of the environmental pollution. J. Hyg. Epidem. Microb. Imm., 30: 27-32.

Paulsson K., Lundbergh K. 1989. The selenium method for treatment of lakes for elevated levels of mercury in fish. Sci. Total Environ., 87-88: 495-507.

Perrone L., Moro R., Caroli M., Universit S., Fisiche S., Federico N. 1996. Trace elements in hair of healthy children sampled by age and sex. Biol. Trace Elem. Res., 51: 71-76.

Raab A., Hansen H.R., Zhuang L.Y., Feldmenn J. 2002. Arsenic accumulation and speciation analysis in wool from sheep exposed to arsenosugars. Talanta, 58: 167-176.

Reis L.S.L.S., Pardo P.E., Camargo A., Oba E. 2010. Mineral element and heavy metal poisoning in animals. Int. J. Med. Med. Sci., 1: 560-579.

Rogowska K.A., Monkiewicz J., Grosicki A. 2009. Lead, cadmium, arsenic, copper, and zinc contents in the hair of cattle living in the area contaminated by a copper smelter in 2006-2008. B. Vet. I. Pulawy, 53: 703-706.

Samanta G., Sharma R., Roychowdhury T., Chakraborti D. 2004. Arsenic and other elements in hair, nails, and skinscales of arsenic victims in West Bengal, India. Sci. Total Environ., 326: 33-47.

Sanna E., Liguori A., Palmas L., Sor M.R., Floris G. 2003. Blood and hair lead levels in boys and girls living in two Sardinian towns at different risks of lead pollution. Ecotoxicol. Environ. Saf., 55: 293-299.

Sarmani S. 1987. A study of trace elements concentrations in human hair of some local population in Malaysia. J. Radioanal. Nucl. Chem., 110: 627-632.

Shanker K., Mishra S., Srivastava S., Srivastava R., Dass S., Prakash S., Srivastava M.M. 1996. Study of mercuryselenium (Hg-Se) interactions and their impact on Hg uptake by the radish (Raphanus sativus) plant. Food Chem. Toxic., 34: 883-886.

Shen S., Li X.F., Cullen W.R., Weinfeld M., Le X.C. 2013. Arsenic binding to proteins. Chem. Rev., 113: 7769-7792.

Soudani N., Amara I.B., Sefi M., Boudawara T., Zeghal N. 2011. Effects of selenium on chromium (VI)-induced hepatotoxicity in adult rats. Exp. Toxicol. Pathol., 63: 541-548.

Templeton G.F. 2011. A two-step approach for transforming continuous variables to normal: implications and recommendations for IS research. Commun. Assoc. Inf. Syst., 28: 41-58.

Underwood E.J., Suttle N.F. 1999. ‘The mineral nutrition of livestock (3rd ed.)’. CAB International: Wallingford, UK. 343-373.

Valko M., Morris H., Cronin M.T.D. 2005. Metals, toxicity and oxidative stress. Curr. Med. Chem., 12: 1161-1208.

Waegeneers N., Pizzolon J.C., Hoenig M., De Temmerman L. 2009. Accumulation of trace elements in cattle from rural and industrial areas in Belgium. Food Addit. Contam. A, 26: 326-332.

Wangher P.D. 2001. Selenium and the brain: a review. Nutr. Neurosci., 4: 81-97.

Xing R., Li Y., Zhang B., Li H., Liao X. 2017. Indicative and complementary effects of human biological indicators for heavy metal exposure assessment. Environ. Geochem. Hlth., 39: 1031-1043.

Zoidis E., Pappas A.C., Georgiou C.A., Komaitis Ε., Feggeros K. 2010. Selenium affects the expression of GPx4 and catalase in the liver of chicken. Comp. Biochem. Physiol. B, 155: 294-300.

Żukowska J., Biziuk M. 2008. Methodological evaluation of method for dietary heavy metal intake. J. Food Sci., 73: 21-29.

Abstract Views

Metrics Loading ...

Metrics powered by PLOS ALM


 Universitat Politècnica de València


Official journal of the World Rabbit Science Association (WRSA)


e-ISSN: 1989-8886     ISSN: 1257-5011