Environmental Science and Pollution Research

, Volume 24, Issue 30, pp 23666–23678 | Cite as

Effects of sex on the levels of metals and metalloids in the hair of a group of healthy Spanish adolescents (13 to 16 years old)

  • Antonio Peña-Fernández
  • Maria del Carmen Lobo-Bedmar
  • Maria José González-Muñoz
Research Article


Human biomonitoring can be a reliable tool to protect the health of the citizens of major urban environments. Human hair may be an invaluable specimen to determine chronic exposure to any environmental contaminant in an individual, especially in the young population. However, different factors including a lack of studies that have established reference values for metals and metalloids (trace elements) in human scalp hair make the use of this matrix controversial. A monitoring study was performed to establish possible normal or tentative reference values of Al, As, Be, Cd, Cr, Cu, Hg, Mn, Pb, Sn, Ti, Tl and Zn in adolescents’ (aged 13–16) hair who have lived since birth in Alcalá de Henares, Madrid region (Spain). Strict inclusion criteria were followed to study the effect of sex on the hair metal content, and the levels of the above contaminants were also studied in park topsoils from Alcalá de Henares. Scalp hair samples were collected from 96 healthy adolescents (28 boys and 68 girls), and reference values were calculated following the recommendations of the International Union of Pure and Applied Chemistry. The levels of Cd, Cu, Pb, Sn and Zn in hair of adolescents from Alcalá de Henares show a sex dependency, being significantly higher in female participants. Sex should be a factor taken into account when developing future reference values and hair metal content. Soil metal contamination was not correlated with the levels found in hair. To conclude, the values of metals and metalloids here analysed and discussed could be considered as tentative reference values for Spanish adolescents aged 13–16 years living in the Madrid region, and may be used to identify the level of exposure of adolescents in this Spanish region to the various metals and metalloids.


Biomonitoring Metals and metalloids Human hair Adolescents Reference values Spain 



In memoriam of Prof. Salvador Granero.

The authors report no financial interests or potential conflicts of interest. The above work is part of a doctoral thesis (Peña-Fernández 2011) which has been funded through the programme EIADES: “Technology Assessment and Remediation of Contaminated Sites” S0505/AMB-0296 and S2009/AMB-1478, Consejería de Educación, Comunidad de Madrid, Spain.

The authors would like to express their sincere appreciation to Mark D. Evans, De Montfort University, for proof reading.

Compliance with ethical standards

The guidelines of the Helsinki Declaration were followed to perform this study.


  1. Aelion CM, Davis HT, McDermott S, Lawson AB (2009) Soil metal concentrations and toxicity: associations with distances to industrial facilities and implications for human health. Sci Total Environ 407:2216–2223CrossRefGoogle Scholar
  2. Afridi HI, Kazi TG, Talpur FN, Brabazon D (2015) Evaluation of trace and toxic elements in the samples of different cigarettes and their impact on human health of Irish diabetes mellitus patients. Clin Lab 61(1–2):123–140Google Scholar
  3. Armbruster DA, Pry T (2008) Limit of blank, limit of detection and limit of quantitation. Clin Biochem Rev 29(Suppl 1):S49–S52Google Scholar
  4. Arvanitidou V, Voskaki I, Tripsianis G, Athanasopoulou H et al (2007) Serum copper and zinc concentrations in healthy children aged 3-14 years in Greece. Biol Trace Elem Res 115(1):1–12CrossRefGoogle Scholar
  5. Avino P, Capannesi G, Renzi L, Rosada A (2013) Instrumental neutron activation analysis and statistical approach for determining baseline values of essential and toxic elements in hairs of high school students. Ecotoxicol Environ Saf 92:206–214CrossRefGoogle Scholar
  6. Bárány E, Bergdahl IA, Bratteby LE, Lundh T et al (2002) Trace elements in blood and serum of Swedish adolescents: relation to gender, age, residential area, and socioeconomic status. Environ Res 89(1):72–84CrossRefGoogle Scholar
  7. Batáriová A, Spevácková V, Benes B, Cejchanová M, Smíd J, Cerná M (2006) Blood and urine levels of Pb, Cd and Hg in the general population of the Czech Republic and proposed reference values. Int J Hyg Enviorn Health 209(4):359–366CrossRefGoogle Scholar
  8. Becker K, Schroeter-Kermani C, Seiwert M, Rϋther M et al (2013) German health-related environmental monitoring: assessing time trends of the general population’s exposure to heavy metals. Int J Hyg Environ Health 216(3):250–254CrossRefGoogle Scholar
  9. Beneš B, Sladká J, Spěváčková V, Šmíd J (2003) Determination of normal concentration levels of Cd, Cr, Cu, Hg, Pb. Se and Zn in hair of the child population in the Czech Republic Cent Eur J Publ Health 11(4):184–186Google Scholar
  10. Bosque MA, Domingo JL, Llobet JM, Corbella J (1991) Cadmium in hair of school children living in Tarragona Province, Spain. Relationship to age, sex, and environmental factors. Biol Trace Elem Res 28(2):147–155CrossRefGoogle Scholar
  11. Budtz-Jørgensen E, Grandjean P, Jørgensen PJ, Weihe P, Keiding N (2004) Association between mercury concentrations in blood and hair in methylmercury-exposed subjects at different ages. Environ Res 95:385–393CrossRefGoogle Scholar
  12. Callan AC, Winsters M, Barton C, Boyce M, Hinwood AL (2012) Children’s exposure to metals: a community-initiated study. Arch Environ Contam Toxicol 62(4):714–722CrossRefGoogle Scholar
  13. Castaño A, Cutanda F, Esteban M, Pärt P, Navarro C et al (2015) Fish consumption patterns and hair mercury levels in children and their mothers in 17 EU countries. Environ Res 141:58–68CrossRefGoogle Scholar
  14. Casteleyn L, Dumez B, Becker K, Kolossa-Gehring M, Den Hond E et al (2015) A pilot study on the feasibility of European harmonized human biomonitoring: strategies towards a common approach, challenges and opportunities. Environ Res 141:3–14CrossRefGoogle Scholar
  15. CDC (2017) National report on human exposure to environmental chemicals, updated tables. Centers for Disease Control and Prevention, AtlantaGoogle Scholar
  16. Chłopicka J, Zachwieja Z, Zagrodzki P, Frydrych J, Słota P, Krośniak M (1998) Lead and cadmium in the hair and blood of children from a highly industrial area in Poland. Biol Trace Elem Res 62:229–234CrossRefGoogle Scholar
  17. Creason JP, Hinners TA, Bumgarner JE, Pinkert C (1975) Trace elements in hair, as a related to exposure in metropolitan New York. Clin Chem 21(4):603–612Google Scholar
  18. Demetriades A, Li X, Ramsey MH, Thornton I (2010) Chemical speciation and bioaccessibility of lead in surface soil and house dust, Lavrion urban area, Attiki. Hellas Environ Geochem Health 32(6):529–552CrossRefGoogle Scholar
  19. Dunicz-Sokolowska A, Graczyk A, Radomska K, Długaszek M, Wlaźlak E, Surkont G (2006) Contents of bioelements and toxic metals in the Polish population determined by hair analysis. Part II. Young persons aged 10-20 years. Magnes Res 19(3):167–179Google Scholar
  20. Ewers U, Krause C, Schulz C, Wilhelm M (1999) Reference values and human biological monitoring values for environmental toxins. Int Arch Occup Environ Health 72:255–260CrossRefGoogle Scholar
  21. Farzin L, Amiri M, Shams H, Ahmadi Faghih MA, Moassesi ME (2008) Blood levels of lead, cadmium, and mercury in residents of Tehran. Biol Trace Elem Res 123(1–3):14–26CrossRefGoogle Scholar
  22. Ferré-Huguet N, Nadal M, Schuhmacher M, Domingo JL (2009) Monitoring metals in blood and hair of the population living near a hazardous waste incinerator: temporal trend. Biol Trace Elem Res 128(3):191–199CrossRefGoogle Scholar
  23. Freire C, Ramos R, López-Espinosa MJ, Díez S, Vioque J, Ballester D, Fernández MF (2010) Hair mercury levels, fish consumption, and cognitive development in preschool children from Granada. Spain. Environ. Res. 110:96–104CrossRefGoogle Scholar
  24. German Federal Environment Agency (2008) German environmental survey on children 2003/06 (GerES IV). Federal Environment Agency (Umweltbundesamt)/Dessau-Roßlau Robert Koch-Institut (RKI), BerlinGoogle Scholar
  25. Gong M, Wu L, Bi XY, Ren LM, Wang L, Ma ZD, Bao ZY, Li ZG (2010) Assessing heavy-metal contamination and sources by GIS-based approach and multivariate analysis of urban-rural topsoils in Wuhan, central China. Environ Geochem Health 32:59–72CrossRefGoogle Scholar
  26. Gonzalez MJ, Rico MC, Hernandez LM, Baluja G (1985) Mercury in human hair: a study of residents in Madrid. Spain Arch Environ Health 40(4):225–228CrossRefGoogle Scholar
  27. González-Muñoz MJ, Peña A, Meseguer I (2008) Monitoring heavy metal contents in food and hair in a sample of young Spanish subjects. Food Chem Toxicol 46:3048–3052CrossRefGoogle Scholar
  28. Granero S, Llobet JM, Schuhmacher M, Corbella J, Domingo JL (1998) Biological monitoring of environmental pollution and human exposure to metals in Tarragona Spain I Levels in hair of school children. Trace Elem Electrol 15(1):39–43Google Scholar
  29. Kasai Y, Iida R, Uchida A (2003) Metal concentrations in the serum and hair of patients with titanium alloy spinal implants. Spine 28(12):1320–1326Google Scholar
  30. Khalique A, Ahmad S, Anjum T, Jaffar M, Shah MH, Shaheen N, Tariq SR, Manzoor S (2005) A comparative study based on gender and age dependence of selected metals in scalp hair. Environ Monit Assess 104(1–3):45–57CrossRefGoogle Scholar
  31. Kilic E, Saraymen R, Demiroglu A, Ok E (2004) Chromium and manganese levels in the scalp hair of normals and patients with breast cancer. Biol Trace Elem Res 102(1–3):19–25CrossRefGoogle Scholar
  32. Kippler M, Goessler W, Nermell B, Ekström EC, Lönnerdal B, El Arifeen S, Vahter M (2009) Factors influencing intestinal cadmium uptake in pregnant Bangladeshi women: a prospective cohort study. Environ Res 109(7):914–921CrossRefGoogle Scholar
  33. Kordas K, Queirolo EI, Ettinger A, Wright RO, Stoltzfus RJ (2010) Prevalence and predictors of exposure to multiple metals in preschool children from Montevideo. Uruguay Sci Total Environ 408(20):4488–4494CrossRefGoogle Scholar
  34. Lech T (2002) Lead, copper, zinc, and magnesium content in hair of children and young people with some neurological diseases. Biol Trace Elem Res 85:111–126CrossRefGoogle Scholar
  35. Li Y, Yang L, Wang W, Li H, Lv J, Zou X (2011) Trace element concentrations in hair of healthy Chinese centenarians. Sci Total Environ 409(8):1385–1390CrossRefGoogle Scholar
  36. Liu X, Cheng J, Song Y, Honda S, Wang L, Liu Z, Sakamoto M, Liu Y (2008) Mercury concentration in hair samples from Chinese people in coastal cities. J Environ Sci 20:1258–1262CrossRefGoogle Scholar
  37. Martí-Cid R, Llobet JM, Castell V, Domingo JL (2008) Dietary intake of arsenic, cadmium, mercury, and lead by the population of Catalonia, Spain. Biol Trace Elem Res 125(2):120–132CrossRefGoogle Scholar
  38. Martínez-Gómez D, Welk GJ, Calle ME, Marcos A, Veiga OL, AFINOS Study Group (2009) Preliminary evidence of physical activity levels measured by accelerometer in Spanish adolescents: the AFINOS Study. Nutr Hosp 24(2):226–232Google Scholar
  39. Martorell I, Perelló G, Martí-Cid R, Llobet JM, Castell V, Domingo JL (2011) Human exposure to arsenic, cadmium, mercury, and lead from foods in Catalonia, Spain: temporal trend. Biol Trace Elem Res 142(3):309–322CrossRefGoogle Scholar
  40. Molina-Villalba I, Lacasaña M, Rodríguez-Barranco M, Hernández AF et al (2015) Biomonitoring of arsenic, cadmium, lead, manganese and mercury in urine and hair of children living near mining and industrial areas. Chemosphere 124:83–91CrossRefGoogle Scholar
  41. Mortada WI, Sobh MA, El-Defrawy MM, Farahat SE (2002) Reference intervals of cadmium, lead, and mercury in blood, urine, hair, and nails among residents in Mansoura City, Nile Delta, Egypt. Environ Res 90(2):104–110CrossRefGoogle Scholar
  42. Nadal M, Bocio A, Schuhmacher M, Domingo JL (2005a) Monitoring metals in the population living in the vicinity of a hazardous waste incinerator Levels in hair of school children. Biol Trace Elem Res 104:203–213CrossRefGoogle Scholar
  43. Nadal M, Bocio A, Schuhmacher M, Domingo JL (2005b) Trends in the levels of metals in soils and vegetation samples collected near a hazardous waste incinerator. Arch Environ Contam Toxicol 49:290–298CrossRefGoogle Scholar
  44. Nowak B, Chmielnicka J (2000) Relationship of lead and cadmium to essential elements in hair, teeth, and nails of environmentally exposed people. Ecotoxicol Environ Saf 46(3):265–274CrossRefGoogle Scholar
  45. NRC (National Research Council) (2000) Committee on the toxicological effects of methyl mercury. National Academies Press, Washington, DCGoogle Scholar
  46. Olivero J, Johnson B, Arguello E (2002) Human exposure to mercury in San Jorge River basin, Colombia (South America). Sci Total Environ 289:41–47CrossRefGoogle Scholar
  47. Özden TA, Gökçay G, Ertem HV, Süoğlu ÖD, Kiliç A, Sökücü S, Saner G (2007) Elevated hair levels of cadmium and lead in school children exposed to smoking and in highways near schools. Clin Bio 40:52–56CrossRefGoogle Scholar
  48. Peña-Fernández, A., 2011. Presencia y distribución medioambiental de metales pesados y metaloides en Alcalá de Henares, Madrid. Evaluación del riesgo para la población y biomonitorización de la población escolar. PhD Thesis. University of Alcalá. Available at:
  49. Peña-Fernández A, Lobo-Bedmar MC, González-Muñoz MJ (2014a) Monitoring of lead in hair of children and adolescents of Alcalá de Henares, Spain A study by gender and residential areas. Environ Int 72:170–175CrossRefGoogle Scholar
  50. Peña-Fernández A, González-Muñoz MJ, Lobo-Bedmar MC (2014b) “Reference values” of trace elements in the hair of a sample group of Spanish children (aged 6-9 years) - are urban topsoils a source of contamination? Pharmacol Environ Toxicol 38(1):141–152CrossRefGoogle Scholar
  51. Peña-Fernández A, González-Muñoz MJ, Lobo-Bedmar MC (2014c) Establishing the importance of human health risk assessment for metals and metalloids in urban environments. Environ Int 72:176–185CrossRefGoogle Scholar
  52. Pereira R, Ribeiro R, Gonçalves F (2004) Scalp hair analysis as a tool in assessing human exposure to heavy metals (S. Dominos mine, Portugal). Sci Total Environ 327(1–3):81–92CrossRefGoogle Scholar
  53. Perelló G, Llobet JM, Gómez-Catalán J, Castell V, Centrich F, Nadal M, Domingo JL (2014) Human health risks derived from dietary exposure to toxic metals in Catalonia, Spain: temporal trend. Biol Trace Elem Res 162(1–3):26–37CrossRefGoogle Scholar
  54. Perelló G, Vicente E, Castell V, Llobet JM, Nadal M, Domingo JL (2015) Dietary intake of trace elements by the population of Catalonia (Spain): results from a total diet study. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32(5):748–755Google Scholar
  55. Perrone L, Moro R, Caroli M, di Toro R, Gialanella G (1996) Trace elements in hair of healthy children sampled by age and sex. Biol Trace Elem Res 51:71–76CrossRefGoogle Scholar
  56. Poulsen OM, Holst E, Christensen JM (1997) Calculation and application of coverage intervals for biological reference values—a supplement to the approved IFCC recommendation (1987) on the theory of reference values. Pure Appl Chem 69(7):1601–1611Google Scholar
  57. Reis AT, Rodrigues SM, Araújo C, Coelho JP et al (2009) Mercury contamination in the vicinity of a chlor-alkali plant and potencial risks to local population. Sci Total Environ 407:2689–2700CrossRefGoogle Scholar
  58. Rubio C, Hardisson A, Reguera JI, Revert C, Lafuente MA, González-Iglesias T (2006) Cadmium dietary intake in the Canary Islands. Spain Environ Res 100:123–129CrossRefGoogle Scholar
  59. Sabbioni E, Goetz L, Birattari C, Bonardi M (1981) Environmental biochemistry of current environmental levels of heavy metals: preparation of radiotracers with very high specific radioactivity for metallobiochemical experiments on laboratory animals. Sci Total Environ 17(3):257–276CrossRefGoogle Scholar
  60. Sakai T, Wariishi M, Nishiyama K (2000) Changes in trace element concentrations in hair of growing children. Biol Trace Elem Res 77:43–51CrossRefGoogle Scholar
  61. Schuhmacher M, Domingo JL, Llobet JM, Corbella J (1991) Lead in children’s hair, as related to exposure in Tarragona Province. Spain Sci Total Environ 104:167–173CrossRefGoogle Scholar
  62. Schuhmacher M, Bellés M, Rico A, Domingo JL, Corbella J (1996) Impact of reduction of lead in gasoline on the blood and hair lead levels in the population of Tarragona Province, Spain, 1990-1995. Sci Total Environ 184:203–209CrossRefGoogle Scholar
  63. Schulz C, Angerer J, Ewers U, Heudorf U, Wilhelm M, on behalf of the Human Biomonitoring Commission of the German Federal Environment Agency (2009) Revised and new reference values for environmental pollutants in urine or blood of children in Germany derived from the German Environmental Survey on Children 2003-2006 (GerES IV). Int J Hyg Environ Health 212:637–647CrossRefGoogle Scholar
  64. Seifert B, Becker K, Helm D, Krause C, Schulz C, Seiwert M (2000) The German Environmental Survey 1990/1992 (GerEs II): reference concentrations of selected environmental pollutants in blood, urine, hair, house dust, drinking water and indoor air. J Exp Anal Environ Epidemiol 10:552–565CrossRefGoogle Scholar
  65. Štupar J, Dolinsek F, Erzen I (2007) Hair-Pb longitudinal profiles and blood-Pb in the population of young Slovenian males. Ecotoxicol Environ Saf 68:134–143CrossRefGoogle Scholar
  66. Tamburo E, Varrica D, Dongarrà G (2015) Coverage intervals for trace elements in human scalp hair are site specific. Environ Toxicol Pharmacol 39(1):70–76CrossRefGoogle Scholar
  67. Tamburo E, Varrica D, Dongarrà G (2016) Gender as a key factor in trace metal and metalloid content of human scalp hair A multi-site study. Sci Total Environ 573:996–1002CrossRefGoogle Scholar
  68. Tommaseo-Ponzetta M, Nardi S, Calliari I, Lucchese M (1998) Trace elements in human scalp hair and soil in Irian Jaya. Biol Trace Elem Res 62:199–212CrossRefGoogle Scholar
  69. Tsanaclis L, Wicks JF (2008) Differentiation between drug use and environmental contamination when testing for drugs in hair. Forensic Sci Int 176(1):19–22CrossRefGoogle Scholar
  70. Unkiewicz-Winiarczyk A, Gromysz-Kałkowska K, Szubartowska E (2009) Aluminium, cadmium and lead concentration in the hair of tobacco smokers. Biol Trace Elem Res 132(1–3):41–50CrossRefGoogle Scholar
  71. Varrica D, Tamburo E, Dongarrà G, Sposito F (2014) Trace elements in scalp hair of children chronically exposed to volcanic activity (Mt. Etna, Italy). Sci. Total Environ 470-471:117–126CrossRefGoogle Scholar
  72. Vienna A, Capucci E, Wolfsperger M, Hauser G (1995) Heavy metal concentration in hair of students in Rome. Anthropol Anz 53(1):27–32Google Scholar
  73. Vrijens J, Leermakers M, Stalpaert M, Schoeters G, Den Hond E et al (2014) Trace metal concentrations measured in blood and urine of adolescents in Flanders, Belgium: reference population and case studies Genk-Zuid and Menen. Int J Hyg Environ Health 217(4–5):515–527CrossRefGoogle Scholar
  74. Wang CT, Li YJ, Wang FJ, Shi YM, Lee BT (2008) Correlation between the iron, magnesium, potassium and zinc content in adolescent girl’s hair and their academic records. Chang Gung Med. J 31(4):358–363Google Scholar
  75. WHO (1990) IPCS. Environmental Health Criteria. Methylmercury, Geneva, p 101Google Scholar
  76. Wolfsperger M, Hauser G, Göβler W, Schlagenhaufen C (1994) Heavy metals in human hair samples from Australia and Italy: influence of sex and smoking habits. Sci Total Environ 156:235–242CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Faculty of Health and Life Sciences, School of Allied Health SciencesDe Montfort UniversityLeicesterUK
  2. 2.Unidad de Toxicología, Departamento de Ciencias BiomédicasUniversidad de AlcaláAlcalá de HenaresSpain
  3. 3.Departamento de Investigación AgroambientalIMIDRAAlcalá de HenaresSpain

Personalised recommendations