Abstract
The objective of the study was to investigate hair trace elements content in children suffering from autism spectrum disorder (ASD). A total of 74 ASD children and 74 sex- and age-matched controls divided into two age groups (2–4 and 5–9 years) were investigated. Hair trace elements content was assessed using inductively coupled plasma mass spectrometry. A general cohort of ASD children was characterized by 29 %, 41 %, and 24 % lower hair levels of chromium (Cr), iodine (I), and vanadium (V), respectively, whereas the level of selenium (Se) exceeded the respective control values by 31 %. In ASD children aged 2–4 years hair Cr, I and V content was 68 %, 36 % and 41 % lower than in the controls. Older ASD children were characterized by 45 % increase in hair Se levels. In a general cohort of ASD children hair beryllium (Be) and tin (Sn) levels were 50 % and 34 % lower than the control values. In the first age group (2–4 years) of ASD children 34 %, 42 %, and 73 % lower levels of arsenic (As), boron (B), and Be were detected. In the second age group of ASD children only a nearly significant 25 % decrease in hair lead (Pb) was detected. Surprisingly, no significant group difference in hair mercury (Hg), zinc (Zn), and copper (Cu) content was detected. Generally, the results of the present study demonstrate that children with ASD are characterized by lower values in hair of not only essential but also toxic trace elements.
Similar content being viewed by others
References
Adams JB, Holloway CE, George F, Quig D (2006) Analyses of toxic metals and essential minerals in the hair of Arizona children with autism and associated conditions, and their mothers. Biol Trace Elem Res 110(3):193–209
Adams JB, Romdalvik J, Ramanujam VM, Legator MS (2007) Mercury, lead, and zinc in baby teeth of children with autism versus controls. J Toxicol Environ Health A 70:1046–1051
Adams JB, Romdalvik J, Levine KE, LW H (2008) Mercury in first-cut baby hair of children with autism versus typically-developing children. Toxicol Environ Chem 90:739–753
Adams JB, Baral M, Geis E, Mitchell J, Ingram J, Hensley A, Zappia I, Newmark S, Gehn E, Rubin RA, Mitchell K, Bradstreet J, Mitchell K (2009) The severity of autism is associated with toxic metal body burden and red blood cell glutathione levels. J Toxicol 2009:532640. doi:10.1155/2009/532640
Adams JB, Audhya T, McDonough-Means S, Rubin RA, Quig D, Geis E, Gehn E, Loresto M, Mitchell J, Atwood S, Barnhouse S, Lee W (2013) Toxicological status of children with autism vs. neurotypical children and the association with autism severity. Biol Trace Elem Res 151:171–180
Al-Ayadhi LY (2005) Heavy metals and trace elements in hair samples of autistic children in Central Saudi Arabia. Neurosciences (Riyadh, Saudi Arabia) 10(3):213–218
Al-Farsi YM, Waly MI, Al-Sharbati MM, Al-Shafaee MA, Al-Farsi OA, Al-Khaduri MM, Gupta I, Ouhtit A, Al-Adawi S, Al-Said MF, Deth RC (2013) Levels of heavy metals and essential minerals in hair samples of children with autism in Oman: a case-control study. Biol Trace Elem Res 151:181–186
APA - American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders: DSM-5. APA, Arlington
Arita A, Costa M (2009) Epigenetics in metal carcinogenesis: nickel, arsenic, chromium and cadmium. Metallomics 1:222–228
Batzevich VA (1995) Hair trace element analysis in human ecology studies. Sci Total Environ 164:89–98
Bertrand J, Mars A, Boyle C, Bove F, Yeargin-Allsopp M, Decoufle P (2001) Prevalence of autism in a United States population: the brick township, New Jersey, investigation. Pediatrics 108:1155–1161
Bjørklund G (2013) The role of zinc and copper in autism spectrum disorders. Acta Neurobiol Exp 73:225–236
Blaurock-Busch E, Amin OR, Rabah T (2011) Heavy metals and trace elements in hair and urine of a sample of Arab children with autistic spectrum disorder. Maedica (Buchar) 6(4):247–257
Blaurock-Busch E, Amin OR, Dessoki HH, Rabah T (2012) Toxic metals and essential elements in hair and severity of symptoms among children with autism. Maedica: a journal of. Clinical Medicine 7:38–48
Błażewicz A, Makarewicz A, Korona-Glowniak I, Dolliver W, Kocjan R (2016) Iodine in autism spectrum disorders. J Trace Elem Med Biol 34:32–33
Chojnacka K, Zielińska A, Górecka H, Dobrzański Z, Górecki H (2010) Reference values for hair minerals of Polish students. Environ Toxicol Phar 29(3):314–319
Ciesielski T, Weuve J, Bellinger DC, Schwartz J, Lanphear B, Wright RO (2012) Cadmium exposure and neurodevelopmental outcomes in U.S. Children. Environ Health Persp 120:758–763
Clarkson TW (1993) Mercury: major issues in environmental health. Environ Health Persp 100:31–38
Crăciun EC, Bjørklund G, Tinkov AA, Urbina MA, Skalny AV, Rad F, Dronca E (2016) Evaluation of whole blood zinc and copper levels in children with autism spectrum disorder. Metab Brain Dis. doi:10.1007/s11011–016–9823-0
Desoto MC, Hitlan RT (2007) Blood levels of mercury are related to diagnosis of autism: a reanalysis of an important data set. J Child Neurol 22:1308–1311
Elsheshtawy E, Tobar S, Sherra K, Atallah S, Elkasaby R (2011) Study of some biomarkers in hair of children with autism. Middle East. Curr Psychiatry 18:6–10
Endreffy I, Bjørklund G, Dicső F, Urbina MA, Endreffy E (2016) Acid glycosaminoglycan (aGAG) excretion is increased in children with autism spectrum disorder, and it can be controlled by diet. Metab Brain Dis 31:273–278
Faber S, Zinn GM, Kern JC 2nd, Kingston HM (2009) The plasma zinc/serum copper ratio as a biomarker in children with autism spectrum disorders. Biomarkers 14:171–180
Fido A, Al-Saad S (2005) Toxic trace elements in the hair of children with autism. Autism 9(3):290–298
Geier DA, Kern JK, King PG, Sykes LK, Geier MR (2012) Hair toxic metal concentrations and autism spectrum disorder severity in young children. Int J Environ Res Public Health 9:4486–4497
Golubkina NA, Alfthan GV (1999) The human selenium status in 27 regions of Russia. J Trace Elem Med Biol 13:15–20
Gorbachev AL, Skalnaya MG, Veldanova MV, Grabeklis AR, Skalny AV (2007) Iodine content in hair as anindicator of body iodine status. Trace Elem Med 8:17–19
Hamza RT, Hewedi DH, Sallam MT (2013) Iodine deficiency in Egyptian autistic children and their mothers: relation to disease severity. Arch Med Res 44(7):555–561
Holmes AS, Blaxill MF, Haley BE (2003) Reduced levels of mercury in first baby haircuts of autistic children. Int J Toxicol 22(4):277–285
Jakovcevski M, Akbarian S (2012) Epigenetic mechanisms in neurological disease. Nat Med 18:1194–1204
James SJ, Cutler P, Melnyk S, Jernigan S, Janak L, Gaylor DW, Neubrander JA (2004) Metabolic biomarkers of increased oxidative stress and impaired methylation capacity in children with autism. Am J Clin Nutr 80:1611–1617
James SJ, Shpyleva S, Melnyk S, Pavliv O, Pogribny IP (2013) Complex epigenetic regulation of engrailed-2 (EN-2) homeobox gene in the autism cerebellum. Transl Psychiat 3:e232. doi:10.1038/tp.2013.8
Jin YH, Clark AB, Slebos RJ, Al-Refai H, Taylor JA, Kunkel TA, Resnick MA, Gordenin DA (2003) Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat Genet 34:239–241
Kern JK, Jones AM (2006) Evidence of toxicity, oxidative stress, and neuronal insult in autism. J Toxicol Environ Health B 9:485–499
Kern JK, Grannemann BD, Trivedi MH, Adams JB (2007) Sulfhydryl-reactive metals in autism. J Toxicol Environ Health A 70:715–721
Kern JK, Geier DA, Deth RC, Sykes LK, Hooker BS, Love JM, Bjørklund G, Chaigneau CG, Haley BE, Geier MR (2015) Systematic assessment of research on autism spectrum disorder and mercury reveals conflicts of interest and the need for transparency in autism research. Sci Eng Ethics. doi:10.1007/s11948–015–9713-6
Kosanovic M, Jokanovic M (2011) Quantitative analysis of toxic and essential elements in human hair. Clinical validity of results. Environ Monit Assess 174(1–4):635–643
Lakshmi Priya MD, Geetha A (2011) Level of trace elements (copper, zinc, magnesium and selenium) and toxic elements (lead and mercury) in the hair and nail of children with autism. Biol Trace Elem Res 142(2):148–158
Li SO, Wang JL, Bjørklund G, Zhao WN, Yin CH (2014) Serum copper and zinc levels in individuals with autism spectrum disorders. Neuroreport 25:1216–1220
Lubkowska A, Sobieraj W (2009) Concentrations of magnesium, calcium, iron, selenium, zinc and copper in the hair of autistic children. Trace Elem Electroly 26(2):72–77
Macedoni-Lukšič M, Gosar D, Bjørklund G, Oražem J, Kodrič J, Lešnik-Musek P, Zupančič M, France-Štiglic A, Sešek-Briški A, Neubauer D, Osredkar J (2015) Levels of metals in the blood and specific porphyrins in the urine in children with autism spectrum disorders. Biol Trace Elem Res 163:2–10
Magos L, Clarkson TW (2008) The assessment of the contribution of hair to methyl mercury excretion. Toxicol Lett 182:48–49
Majewska MD, Urbanowicz E, Rok-Bujko P, Namysłowska I, Mierzejewski P (2010) Age-dependent lower or higher levels of hair mercury in autistic children than in healthy controls. Acta Neurobiol Exp 70:196–208
Marlowe, M, Errera, J (1985) Hair mineral content as a predictor of childhood autism. Document Resume Ed 266 601 EC 182 016, 113
Mohamed FE, Zaky EA, Sayed AB, Elhossieny RM, Zahra SS, Eldin WS, Youssef WY, Khaled RA, Youssef AM (2015) Assessment of hair aluminum, lead, and mercury in a sample of autistic Egyptian children: environmental risk factors of heavy metals in autism. Behav Neurol. doi:10.1155/2015/545674
Mostafa GA, Bjørklund G, Urbina MA, Al-Ayadhi LY (2016) The levels of blood mercury and inflammatory-related neuropeptides in the serum are correlated in children with autism spectrum disorder. Metab Brain Dis. doi:10.1007/s11011–015–9784-8
O’Rahilly S (2009) Human genetics illuminates the paths to metabolic disease. Nature 462:307–314
Oster O, Prellwitz W (1990) The renal excretion of selenium. Biol Trace Elem Res 24:119–146
Perera F, Herbstman J (2011) Prenatal environmental exposure, epigenetics, and disease. Reprod Toxicol 31:363–373
Pick D, Leiterer M, Einax JW (2010) Reduction of polyatomic interferences in biological material using dynamic reaction cell ICP-MS. Microchem J 95(2):315–319
Prasad AS (2012) Discovery of human zinc deficiency: 50 years later. J Trace Elem Med Biol 26:66–69
Rossignol DA, Genuis SJ, Frye RE (2014) Environmental toxicants and autism spectrum disorders: a systematic review. Trans Psychiatry 4(2):e360
Shaw CA, Tomljenovic L (2013) Aluminum in the central nervous system (CNS): toxicity in humans and animals, vaccine adjuvants, and autoimmunity. Immunol Res 56:304–316
Shearer TR, Larson K, Neuschwander J, Gedney B (1982) Minerals in the hair and nutrient intake of autistic children. J Autism Dev Disord 12(1):25–34
Simashkova, N, Makarova, L, Grabeklis, A, Skalny, A (2015) Selenium status of children with autistic spectrum disorders. The International Selenium Seminar «Selenium: biology, clinical and preventive medicine, nutrition», Yaroslavl
Skalny AV (2013) Low Se and elevated hair Mn, Cd: a specific feature for autistic children? Trace elements in Medicine 14(4):84
Skalny AV, Skalnaya MG, Bjørklund G, Nikonorov AA, Tinkov AA (2016) Mercury as a possible link between maternal obesity and autism spectrum disorder. Med Hypotheses. doi:10.1016/j.mehy.2016.04.021
Sullivan KM (2009) Iodine deficiency as a cause of autism. Jo Neurol Sci 276(1):202
Takiguchi M, Achanzar WE, Qu W, Li G, Waalkes MP (2003) Effects of cadmium on DNA-(cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp Cell Res 286:355–365
Vinceti M, Mandrioli J, Borella P, Michalke B, Tsatsakis A, Finkelstein Y (2014) Selenium neurotoxicity in humans: bridging laboratory and epidemiologic studies. Toxicol Lett 230(2):295–303
Yassa HA (2014) Autism: a form of lead and mercury toxicity. Environ Toxicol Phar 3(8):1016–1024
Yasuda H, Yonashiro T, Yoshida K, Ishii T, Tsutsui T (2005) Mineral imbalance in children with autistic disorders. BRTE 16(4):285–292
Yorbik Ö, Kurt İ, Haşimi A, Öztürk Ö (2010) Chromium, cadmium, and lead levels in urine of children with autism and typically developing controls. Biol Trace Elem Res 135(1–3):10–15
Zablotsky B, Black LI, Maenner MJ, Schieve LA, Blumberg SJ (2015) Estimated prevalence of autism and other developmental disabilities following questionnaire changes in the 2014 National Health Interview Survey. Natl Health Stat Report 87:1–20
Acknowledgments
This paper was financially supported by the Ministry of Education and Science of the Russian Federation on the program to improve the competitiveness of Peoples’ Friendship University (RUDN) University among the world’s leading research and education centers in 2016 – 2020.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no potential conflicts of interest.
Rights and permissions
About this article
Cite this article
Skalny, A.V., Simashkova, N.V., Klyushnik, T.P. et al. Hair toxic and essential trace elements in children with autism spectrum disorder. Metab Brain Dis 32, 195–202 (2017). https://doi.org/10.1007/s11011-016-9899-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11011-016-9899-6