JNSS 2014, 5(1-2):70-82 | DOI: 10.32725/jnss.2014.008

Neurotoxicity of heavy metals in the light of gender studies

Jiří Patočka
University of South Bohemia, Faculty of Health and Social Studies, Department of Radiology, Toxicology and Civil Protection, České Budějovice, Czech Republic

Gender-related differences regarding susceptibility to chemical exposure to neurotoxicants have not received sufficient attention. Although a significant number of epidemiological studies on the neurodevelopmental effects of metal exposure have been published in the last twenty years, not many of these studies have considered the possible gender-specific effects of such exposure. This review is focused on studies in which the gender differences in pre- and/or postnatal exposures to five metals (mercury, lead, manganese, cadmium, and arsenic) and neurodevelopment were evaluated. A significant number of experimental and epidemiological studies on brain effects of exposure to neurotoxic substances has been published, however not many of them have considered the possible gender-specific effects of such exposure.
Subtle and less subtle differences exist in brain function. They exist due to effects of sex hormones as well as to effects that sex hormones exert on the uterus during development, leading to persisting epigenetic markers. Recent human and animal studies suggest that gender dimorphic profiles are emerging in terms of neurotoxicity, moreover that gender differences in neurotoxicity are more widespread than one may expect. If a risk factor is underestimated in one gender, or if gender specific symptoms are not recognized, timely treatment may be delayed. Knowing that one gender is more vulnerable to poisoning helps to carry out a more effective prevention strategy, that is more efficient than the global approaches. In addition, it has significant consequences on public health concerns and outcomes. Our work is complemented by a critical analysis of some previously published studies.

Keywords: gender; neurotoxicity; heavy metals; children
Grants and funding:

The article was created within the project EPZ2012_003 ZSF JU in České Budějovice.

Received: August 15, 2013; Accepted: February 26, 2014; Published: March 1, 2014  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Patočka J. Neurotoxicity of heavy metals in the light of gender studies. Journal of Nursing, Social Studies, Public Health and Rehabilitation. 2014;5(1-2):70-82. doi: 10.32725/jnss.2014.008.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Abdelouahab N, Mergler D, Takser L, Vanier C, St-Jean M, Baldwin M, Spear PA, Chan HM (2008). Gender differences in the effects of organochlorines, mercury, and lead on thyroid hormone levels in lakeside communities of Quebec (Canada). Environ Res. 107/3: 380-392. Go to original source... Go to PubMed...
    2. Abernethy DR, Destefano AJ, Cecil TL, Zaidi K, Williams RL (2010). USP Metal Impurities Advisory Panel. Metal impurities in food and drugs. Pharm Res. 27/5: 750-755. Go to original source... Go to PubMed...
    3. Aboud AA, Tidball AM, Kumar KK, Neely MD, Ess KC, Erikson KM, Bowman AB (2012). Genetic risk for Parkinson's disease correlates with alterations in neuronal manganem sensitivity between two human subjects. Neurotoxicology. 33/6: 1443-1449. Go to original source... Go to PubMed...
    4. Baghurst PA, McMichael AJ, Wigg NR, Vimpani GV, Robertson EF, Roberts RJ, Tong SL (1992). Environmental exposure to lead and children's intelligence at the age of seven years. The Port Pirie Cohort Study. N Engl J Med. 327/18: 1279-1284. Go to original source... Go to PubMed...
    5. Bardullas U, Limón-Pacheco JH, Giordano M, Carrizales L, Mendoza-Trejo MS, Rodríguez VM (2009). Chronic low-level arsenic exposure causes gender-specific alterations in locomotor activity, dopaminergic systems, and thioredoxin expression in mice. Toxicol Appl Pharmacol. 239/2: 169-177. Go to original source... Go to PubMed...
    6. Bencko V, Cikrt M (1984). Manganese: a review of occupational and environmental toxicology. J Hyg Epidemiol Microbiol Immunol. 28/2: 139-148.
    7. Bertin G, Averbeck D (2006). Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochemie. 88/11: 1549-1559. Go to original source... Go to PubMed...
    8. Boscolo M, Antonucci S, Volpe AR, Carmignani M, Di Gioacchino M (2009). Acute mercury intoxication and use of chelating agents. J Biol Regul Homeost Agents. 23/4: 217-223.
    9. Bouchard MF, Sauvé S, Barbeau B, Legrand M, Brodeur MÈ, Bouffard T, Limoges E, Bellinger DC, Mergler D (2011). Intellectual impairment in school-age children exposed to manganese from drinking water. Environ Health Perspect. 119/1: 138-143. Go to original source... Go to PubMed...
    10. Burns JM, Baghurst PA, Sawyer MG, McMichael AJ, Tong SL (1999). Lifetime low-level exposure to environmental lead and children's emotional and behavioral development at ages 11-13 years. The Port Pirie Cohort Study. Am J Epidemiol. 149/8: 740-749. Go to original source... Go to PubMed...
    11. Cauli O, Piedrafita B, Llansola M, Felipo V (2013). Gender differential effects of developmental exposure to methyl-mercury, polychlorinated biphenyls 126 or 153, or its combinations on motor activity and coordination. Toxicology. 311/1-2: 61-68. Go to original source... Go to PubMed...
    12. Chen Y, Graziano JH, Parvez F, Liu M, Slavkovich V, Kalra T, Argos M, Islam T, Ahmed A, Rakibuz-Zaman M, Hasan R, Sarwar G et al. (2011). Arsenic exposure from drinking water and mortality from cardiovascular disease in Bangladesh: prospective cohort study. BMJ. 342: d2431. Go to original source... Go to PubMed...
    13. Cílek V (1998). Arzen v podzemních vodách Bangladéše [Arsenic in grounwater of Bangladesh]. Vesmír. 77/11: 607 (Czech).
    14. Cooper RG (2006). Effect of tobacco smoking on renal function. Indian J. Med. Res. 124/3: 261-268.
    15. Cordier S, Garel M, Mandereau L, Morcel H, Doineau P, Gosme-Seguret S, Josse D, White R, Amiel-Tison C (2002). Neurodevelopmental investigations among methylmercury-exposed children in French Guiana. Environ Res. 89/1: 1-11. Go to original source... Go to PubMed...
    16. Davidson PW, Myers GJ, Cox C, Axtell C, Shamlaye C, Sloane-Reeves J, Cernichiari E, Needham L, Choi A, Wang Y, Berlin M, Clarkson TW (1998). Effects of prenatal and postnatal methylmercury exposure from fish consumption on neurodevelopment: outcomes at 66 months of age in the Seychelles Child Development Study. JAMA. 280/8: 701-707. Go to original source... Go to PubMed...
    17. Davidson PW, Myers GJ, Shamlaye C, Cox C, Wilding GE (2004). Prenatal exposure to methylmercury and child development: influence of social factors. Neurotoxicol Teratol. 26/4: 553-559. Go to original source... Go to PubMed...
    18. Davidson PW, Jean-Sloane-Reeves, Myers GJ, Hansen ON, Huang LS, Georger LA, Cox C, Thurston SW, Shamlaye CF, Clarkson TW (2008). Association between prenatal exposure to methylmercury and visuospatial ability at 10.7 years in the seychelles child development study. Neurotoxicology. 29/3: 453-459. Go to original source... Go to PubMed...
    19. Davidson PW, Leste A, Benstrong E, Burns CM, Valentin J, Sloane-Reeves J, Huang LS, Miller WA, Gunzler D, van Wijngaarden E, Watson GE, Zareba G et al. (2010). Fish consumption, mercury exposure, and their associations with scholastic achievement in the Seychelles Child Development Study. Neurotoxicology. 31/5: 439-447. Go to original source... Go to PubMed...
    20. de Souza Lisboa SF, Gonçalves G, Komatsu F, Queiroz CA, Almeida AA, Moreira EG (2005). Developmental lead exposure induces depressive-like behavior in female rats. Drug Chem Toxicol. 28/1: 67-77. Go to original source... Go to PubMed...
    21. DENAMIC (2012). Developmental Neurotoxicity Assessment of Mixtures in Children. Grant Agreement No. 282957. [online] [cit. 2013-28-07]. Available from: http://www.patlab.ro/documents/DENAMIC.pdf
    22. Dietrich KN, Ris MD, Succop PA, Berger OG, Bornschein RL (2001). Early exposure to lead and juvenile delinquency. Neurotoxicol Teratol. 23/6: 511-518. Go to original source... Go to PubMed...
    23. Dluzen DE, McDermott JL (2000). Gender differences in neurotoxicity of the nigrostriatal dopaminergic system: implications for Parkinson's disease. J Gend Specif Med. 3/6: 36-42.
    24. Dressler J, Schulz K, Klemm M, Schüttig R, Beuthin A, Felscher D (2002). Lethal manganese-cadmium intoxication. A case report. Arch Toxicol. 76/8: 449-451. Go to original source... Go to PubMed...
    25. Ekstrand J, Nielsen JB, Havarinasab S, Zalups RK, Söderkvist P, Hultman P (2010). Mercury toxicokinetics - dependency on strain and gender. Toxicol Appl Pharmacol. 243/3: 283-291. Go to original source... Go to PubMed...
    26. El-Khatib F, Rauchenzauner M, Lechleitner M, Hoppichler F, Naser A, Waldmann M, Trinka E, Unterberger I, Bauer G, Luef GJ (2007). Valproate, weight gain and carbohydrate craving: A gender study. Europ J Epilepsy 16/3: 226-232. Go to original source... Go to PubMed...
    27. Gao Y, Yan CH, Tian Y, Wang Y, Xie HF, Zhou X, Yu XD, Yu XG, Tong S, Zhou QX, Shen XM. (2007). Prenatal exposure to mercury and neurobehavioral development of neonates in Zhoushan City, China. Environ. Res. 105/3: 390-399. Go to original source... Go to PubMed...
    28. Giménez-Llort L, Ahlbom E, Daré E, Vahter M, Ögren S, Ceccatelli S (2001). Prenatal exposure to methylmercury changes dopamine-modulated motor aktivity during early ontogeny: age and gender-dependent effects. Environ Toxicol Pharmacol. 9/3: 61-70. Go to original source... Go to PubMed...
    29. Goulet S, Doré FY, Mirault ME (2003). Neurobehavioral changes in mice chronically exposed to methylmercury during fetal and early postnatal development. Neurotoxicol Teratol. 25/3: 335-347. Go to original source... Go to PubMed...
    30. Grandjean P, Weihe P, White RF, Debes F (1998). Cognitive performance of children prenatally exposed to "safe" levels of methylmercury. Environ Res. 77/2: 165-172. Go to original source... Go to PubMed...
    31. Hamadani JD, Grantham-McGregor SM, Tofail F, Nermell B, Fängström B, Huda SN, Yesmin S, Rahman M, Vera-Hernández M, Arifeen SE, Vahter M (2010). Pre- and postnatal arsenic exposure and child development at 18 months of age: a cohort study in rural Bangladesh. Int J Epidemiol. 39/5: 1206-1216. Go to original source... Go to PubMed...
    32. Hamadani JD, Tofail F, Nermell B, Gardner R, Shiraji S, Bottai M, Arifeen SE, Huda SN, Vahter M (2011). Critical windows of exposure for arsenic-associated impairment of cognitive function in pre-school girls and boys: a population-based cohort study. Int J Epidemiol. 40/6: 1593-1604. Go to original source... Go to PubMed...
    33. Hassani H, Golbabaei F, Ghahri A, Hosseini M, Shirkhanloo H, Dinari B, Eskandari D, Fallahi M (2012). Occupational exposure to manganese-containing welding fumes and pulmonary function indices among natural gas transmission pipeline welders. J Occup Health. 54/4: 316-322. Go to original source... Go to PubMed...
    34. Holt D, Webb M (1986). The toxicity and teratogenicity of mercuric mercury in the pregnant rat. Arch. Toxicol. 58/4: 243-248. Go to original source... Go to PubMed...
    35. Hout JJ (2012). Lead in drinking water. J. Environ. Health 75/1: 56; author reply 56-57.
    36. Huang CF, Hsu CJ, Liu SH, Lin-Shiau SY (2008). Ototoxicity induced by cinnabar (a naturally occurring HgS) in mice through oxidative stress and down-regulated Na(+)/K(+)-ATPase activities. Neurotoxicology. 29/3: 386-396. Go to original source... Go to PubMed...
    37. Jedrychowski W, Perera F, Jankowski J, Mrozek-Budzyn D, Mroz E, Flak E, Edwards S, Skarupa A, Lisowska-Miszczyk I (2009). Gender specific differences in neurodevelopmental effects of prenatal exposure to very low-lead levels: the prospective cohort study in three-year olds. Early Hum Dev. 85/8: 503-510. Go to original source... Go to PubMed...
    38. Kah M, Levy L, Brown C (2012). Potential for effects of land contamination on human health. 1. The case of cadmium. J. Toxicol. Environ. Health B. Crit. Rev. 15/5: 348-363. Go to original source... Go to PubMed...
    39. Kern JK, Geier DA, Audhya T, King PG, Sykes LK, Geier MR (2012). Evidence of parallels between mercury intoxication and the brain pathology in autism. Acta Neurobiol Exp (Wars). 72/2: 113-153. Go to original source... Go to PubMed...
    40. Khan A, Sulkowski ZL, Chen T, Zavacki AM, Sajdel-Sulkowska EM (2012). Sex-dependent changes in cerebellar thyroid hormone-dependent gene expression following perinatal exposure to thimerosal in rats. J Physiol Pharmacol. 63/3: 277-283.
    41. Kimura M, Miyakawa T, Matsushita S, So M, Higuchi S (2011). Gender Differences in the Effects of ADH1B and ALDH2 Polymorphisms on Alcoholism. Alcohol Clin Exp Res. 35/11: 1923-1927. Go to original source... Go to PubMed...
    42. Kippler M, Tofail F, Hamadani JD, Gardner RM, Grantham-McGregor SM, Bottai M, Vahter M (2012a). Early-life cadmium exposure and child development in 5-year-old girls and boys: a cohort study in rural Bangladesh. Environ Health Perspect. 120/10: 1462-1468. Go to original source... Go to PubMed...
    43. Kippler M, Tofail F, Gardner R, Rahman A, Hamadani JD, Bottai M, Vater M (2012b). Maternal cadmium exposure during pregnancy and size at birth: a prospective cohort study. Environ. Health Perspect. 120/2: 284-289. Go to original source... Go to PubMed...
    44. Kondej D, Gawęda E (2012). Metals in dust fractions emitted at mechanical workstations. Int J Occup Saf Ergon. 18/4: 453-460. Go to original source... Go to PubMed...
    45. Kontur PJ, Fechter LD (1988). Brain regional manganese levels and monoamine metabolism in manganese-treated neonatal rats. Neurotoxicol Teratol. 10/4: 295-303. Go to original source... Go to PubMed...
    46. Krivosheev AB, Poteriaeva EL, Krivosheev BN, Kupriianova LI, Smirnova EL (2012). Toxic effects of cadmium on the human body (literature review). Med Tr Prom Ekol. 6: 35-42 [Article in Russian].
    47. Leasure JL, Giddabasappa A, Chaney S, Johnson JE, Jr., Pothakos K, Lau YS, Fox DA (2008). Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ Health Perspect. 116/3: 355-361. Go to original source... Go to PubMed...
    48. Llop S, Guxens M, Murcia M, Lertxundi A, Ramon R, Riaño I, Rebagliato M, Ibarluzea J, Tardon A, Sunyer J, Ballester F; INMA Project (2012). Prenatal exposure to mercury and infant neurodevelopment in a multicenter cohort in Spain: study of potential modifiers. Am J Epidemiol. 175/5: 451-465. Go to original source... Go to PubMed...
    49. Llop S, Lopez-Espinosa MC, Rebagliato M, Ballester F (2013). Gender differences in the neurotoxicity of metals in children. Toxicology 311/1: 3-12. Go to original source... Go to PubMed...
    50. Madison JL, Wegrzynowicz M, Aschner M, Bowman AB (2011). Gender and manganese exposure interactions on mouse striatal neuron morphology. Neurotoxicology. 32/6: 896-906. Go to original source... Go to PubMed...
    51. Mania M, Wojciechowska-Mazurek M, Starska K, Rebeniak M, Postupolski J (2012). Fish and seafood as a source of human exposure to methylmercury. Rocz Panstw Zakl Hig. 63/3: 257-264 [Article in Polish].
    52. Mansouri MT, Naghizadeh B, López-Larrubia P, Cauli O (2012). Gender-dependent behavioural impairment and brain metabolites in young adult rats after short term exposure to lead acetate. Toxicol Lett. 210/1: 15-23. Go to original source... Go to PubMed...
    53. Miller AA, De Silva TM, Jackman KA, Sobey CG (2007). Effect of gender and sex hormones on vascular oxidative stress. Clin Exp Pharmacol Physiol. 34/10: 1037-1043. Go to original source... Go to PubMed...
    54. Moreno JA, Yeomans EC, Streifel KM, Brattin BL, Taylor RJ, Tjalkens RB (2009). Age-dependent susceptibility to manganese-induced neurological dysfunction. Toxicol. 112/2: 394-404. Go to original source... Go to PubMed...
    55. Murata K, Yoshida M, Sakamoto M, Iwai-Shimada M, Yaginuma-Sakurai K, Tatsuta N, Iwata T, Karita K, Nakai K (2011). Recent evidence from epidemiological studies on methylmercury toxicity. Nihon Eiseigaku Zasshi. 66/4: 682-695. Go to original source... Go to PubMed...
    56. Myers GJ, Thurston SW, Pearson AT, Davidson PW, Cox C, Shamlaye CF, Cernichiari E, Clarkson TW (2009). Postnatal exposure to methyl mercury from fish consumption: a review and new data from the Seychelles Child Development Study. Neurotoxicology. 30/3: 338-349. Go to original source... Go to PubMed...
    57. Olczak M, Duszczyk M, Mierzejewski P, Meyza K, Majewska MD (2011). Persistent behavioral impairments and alterations of brain dopamine system after early postnatal administration of thimerosal in rats. Behav Brain Res. 223/1: 107-118. Go to original source... Go to PubMed...
    58. Onishchenko N, Tamm C, Vahter M, Hökfelt T, Johnson JA, Johnson DA, Ceccatelli S (2007). Developmental exposure to methylmercury alters learning and induces depression-like behavior in male mice. Toxicol Sci. 97/2: 428-437. Go to original source... Go to PubMed...
    59. Palme H, O'Neill HC (2003). Cosmochemical Estimates of Mantle Composition. Treatise on Geochemistry, Volume 2. Editor: Richard W. Carlson. Executive Editors: Heinrich D. Holland and Karl K. Turekian. pp. 568. ISBN 0-08-043751-6. Elsevier, 2003, s. 1-38.
    60. Patočka J (2008). Organic lead toxicology. Acta Medica (Hradec Králové). 51/4: 209-213. Go to original source...
    61. Patočka J, Černý K (2003). Inorganic lead toxicology. Acta Medica (Hradec Králové). 46/2: 65-72. Go to original source...
    62. Patočka J, Zölzer F (2013). Environmentální zdraví: naléhavé problémy [Environmental health: urgent problems]. Kontakt. 15/2: 190-202 (Czech). Go to original source...
    63. Rahman MM, Ng JC, Naidu R (2009). Chronic exposure of arsenic via drinking water and its averse health impacts on humans. Environ Geochem Health. 31 Suppl 1: 189-200. Go to original source... Go to PubMed...
    64. Rathore M, Singh A, Pant VA (2012). The dental amalgam toxicity fear: a myth or actuality. Toxic Int. 19/2: 81-88. Go to original source... Go to PubMed...
    65. Renzetti CM, Curran DJ (2003). Ženy, muži a společnost [Men, women and society]. Praha, Karolinum (Czech).
    66. Riojas-Rodríguez H, Solís-Vivanco R, Schilmann A, Montes S, Rodríguez S, Ríos C, Rodríguez-Agudelo Y (2010). Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ Health Perspect. 118/10: 1465-1470. Go to original source... Go to PubMed...
    67. Ris MD, Dietrich KN, Succop PA, Berger OG, Bornschein RL (2004). Early exposure to lead and neuropsychological outcome in adolescence. J Int Neuropsychol Soc. 10/2: 261-270. Go to original source... Go to PubMed...
    68. Riva MA, Lafranconi A, D'Orso MI, Cesana G (2012). Lead poisoning: historical aspects of a paradigmatic "occupational and environmental disease". Saf Health Work. 3/1: 11-16. Go to original source... Go to PubMed...
    69. Roels HA, Bowler RM, Kim Y, Claus Henn B, Mergler D, Hoet P, Gocheva VV, Bellinger DC, Wright RO, Harris MG, Chang Y, Bouchard MF et al. (2012). Manganese exposure and cognitive deficits: a growing concern for manganem neurotoxicity. Neurotoxicology. 33/4: 872-880. Go to original source... Go to PubMed...
    70. Rosado JL, Ronquillo D, Kordas K, Rojas O, Alatorre J, Lopez P, Garcia-Vargas G, Del Carmen Caamaño M, Cebrián ME, Stoltzfus RJ (2007). Arsenic exposure and cognitive performance in Mexican schoolchildren. Environ Health Perspect. 115/9: 1371-1375. Go to original source... Go to PubMed...
    71. Satarug S (2012). Long-term exposure to cadmium in food and cigarette smoke, liver effects and hepatocellular carcinoma. Curr Drug Metab. 13/3: 257-271. Go to original source... Go to PubMed...
    72. Scallet AC, Meredith JM (2002). Quantitative three-dimensional reconstruction: feasibility for studies of sexually dimorphic hypothalamic development in rats. Neurotoxicol Teratol. 24/1: 81-88. Go to original source... Go to PubMed...
    73. Simon P, Dupuis R, Costentin J (1994). Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res. 61/1: 59-64. Go to original source... Go to PubMed...
    74. Singer HS, Denckla MB (1998). Gender study of neuropsychological and neuromotor function in children with Tourette Syndrome with and without attention-deficit hyperactivity disorder. J Child Neurol. 13/6: 277-282. Go to original source... Go to PubMed...
    75. Soeiro AC, Gouvêa TS, Moreira EG (2007). Behavioral effects induced by subchronic exposure to Pb and their reversion are concentration and gender dependent. Hum Exp Toxicol. 26/9: 733-739. Go to original source... Go to PubMed...
    76. Soleo L, Lovreglio P, Panuzzo L, D'Errico MN, Basso A, Gilberti ME, Drago I, Tomasi C, Apostoli P (2012). Health risk assessment of exposure to metals in the workers of the steel foundry and in the general population of Taranto (Italy). G Ital Med Lav Ergon. 34/4: 381-391 [Article in Italian].
    77. Stern L (1981). In vivo assessment of the teratogenic potential of drugs in humans. Obstet. Gynecol. 58(Suppl. 5): 3S-8S.
    78. Sulkowski ZL, Chen T, Midha S, Zavacki AM, Sajdel-Sulkowska EM (2012). Maternal thimerosal exposure results in aberrant cerebellar oxidative stress, thyroid hormone metabolism, and motor behavior in rat pups; sex- and strain-dependent effects. Cerebellum. 11/2: 575-586. Go to original source... Go to PubMed...
    79. Thompson J, Bannigan J (2008). Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol. 25/3: 304-315. Go to original source... Go to PubMed...
    80. Tong S, McMichael AJ, Baghurst PA (2000). Interactions between environmental lead exposure and sociodemographic factors on cognitive development. Arch Environ Health. 55/5: 330-335. Go to original source... Go to PubMed...
    81. Vahter M, Berglund M, Akesson A, Lidén C (2002). Metals and women's health. Environ Res. 88/3: 145-155. Go to original source... Go to PubMed...
    82. Vahter M, Akesson A, Lidén C, Ceccatelli S, Berglund M (2007). Gender differences in the disposition and toxicity of metals. Environ Res. 104/1: 85-95. Go to original source... Go to PubMed...
    83. Vermeir G, Viaene M, Staessen J, Hond ED, Roels HA (2005). Neurobehaviour investigations in adolescents exposed to environmental pollutants. Environ Toxicol Pharmacol. 19/3: 707-713. Go to original source... Go to PubMed...
    84. Vieira MC, Torronteras R, Córdoba F, Canalejo A (2012). Acute toxicity of manganese in goldfish Carassius auratus is associated with oxidative stress and organ specific antioxidant responses. Ecotoxicol Environ Saf. 78: 212-217. Go to original source... Go to PubMed...
    85. Watson GE, Evans K, Thurston SW, van Wijngaarden E, Wallace JM, McSorley EM, Bonham MP, Mulhern MS, McAfee AJ, Davidson PW, Shamlaye CF, Strain JJ et al. (2012). Prenatal exposure to dental amalgam in the Seychelles Child Development Nutrition Study: associations with neurodevelopmental outcomes at 9 and 30 months. Neurotoxicology. 33/6: 1511-1517. Go to original source... Go to PubMed...
    86. Wójcik A, Brzeski Z, Sobańska E, Kargul M, Borzecki A (2004). Hazard estimation for the chosen work stands in metallurgical industry. Ann Univ Mariae Curie Sklodowska Med. 59/2: 416-420.
    87. Yang Y, Ma Y, Ni L, Zhao S, Li L, Zhang J, Fan M, Liang C, Cao J, Xu L (2003). Lead exposure through gestation-only caused long-term learning/memory deficits in young adult offspring. Exp Neurol. 184/1: 489-495. Go to original source... Go to PubMed...
    88. Yin Z, Milatovic D, Aschner JL, Syversen T, Rocha JB, Souza DO, Sidoryk M, Albrecht J, Aschner M (2007). Methylmercury induces oxidative injury, alterations in permeability and glutamine transport in cultured astrocytes. Brain Res. 1131/1: 1-10. Go to original source... Go to PubMed...
    89. Yoshida M, Watanabe C, Horie K, Satoh M, Sawada M, Shimada A (2005). Neurobehavioral changes in metallothionein-null mice prenatally exposed to mercury vapor. Toxicol Lett. 155/3: 361-368. Go to original source... Go to PubMed...
    90. Youness ER, Mohammed NA, Morsy FA (2012). Cadmium impact and osteoporosis: mechanism of action. Toxicol Mech Methods. 22/7: 560-567. Go to original source... Go to PubMed...
    91. Young RJ, Critchley JA, Young KK, Freebairn RC, Reynolds AP, Lolin YI (1996). Fatal acute hepatorenal failure following potassium permanganate ingestion. Hum Exp Toxicol. 15/3: 259-261. Go to original source... Go to PubMed...
    92. Zabłocka-Słowińska K, Grajeta H (2012). The role of manganese in ethiopatogenesis and prevention of selected diseases. Postepy Hig Med Dosw (Online). 66: 549-553. Go to original source... Go to PubMed...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content