Human predisposition to cognitive impairment and its relation with environmental exposure to potentially toxic elements

Abstract

New lines of evidence suggest that less than 10% of neurodegenerative diseases have a strict genetic aetiology and other factors may be prevalent. Environmental exposures to potentially toxic elements appear to be a risk factor for Parkinson’s, Alzheimer’s and sclerosis diseases. This study proposes a multidisciplinary approach combining neurosciences, psychology and environmental sciences while integrating socio-economic, neuropsychological, environmental and health data. We present the preliminary results of a neuropsychological assessment carried out in elderly residents of the industrial city of Estarreja. A battery of cognitive tests and a personal questionnaire were administered to the participants. Multivariate analysis and multiple linear regression analysis were used to identify potential relationships between the cognitive status of the participants and environmental exposure to potentially toxic elements. The results suggest a relationship between urinary PTEs levels and the incidence of cognitive disorders. They also point towards water consumption habits and profession as relevant factors of exposure. Linear regression models show that aluminium (R 2 = 38%), cadmium (R 2 = 11%) and zinc (R 2 = 6%) are good predictors of the scores of the Mini-Mental State Examination cognitive test. Median contents (µg/l) in groundwater are above admissible levels for drinking water for aluminium (371), iron (860), manganese (250), and zinc (305). While the World Health Organization does not provide health-based reference values for aluminium, results obtained from this study suggest that it may have an important role in the cognitive status of the elderly. Urine proved to be a suitable biomarker of exposure both to elements with low and high excretion rates.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Afridi, H. I., Kazi, T. G., Kazi, N., Jamali, M. K., Arain, M. B., Jalbani, N., Baig, J. A., & Sarfraz, R. A. (2008). Evaluation of status of toxic metals in biological samples of diabetes mellitus patients. Diabetes research and clinical practice, 80(2), 280–288.

    CAS  Article  Google Scholar 

  2. Ahlskog, J. E. (2016). New and appropriate goals for parkinson disease physical therapy. JAMA Neurology, 73(3), 1–2.

    Article  Google Scholar 

  3. APA. (2016). Programa Operacional Temático Valorização do Território Eixo Prioritário III. Recuperação do Passivo Ambiental. Documento Enquadrador. https://poseur.portugal2020.pt/media/38027/01_docenq_passivoambiental.pdf.

  4. Ashok, A., Rai, N. K., Tripathi, S., & Bandyopadhyay, S. (2014). Exposure to As-, Cd-, and Pb-mixture induces Aβ, amyloidogenic APP processing and cognitive impairments via oxidative stress-dependent neuroinflammation in young rats. Toxicological Sciences, kfu208.

  5. Benzecri, F. (1980). Introduction à l’analyse des correspondances d’après un exemple de données médicales. Les cahiers de l’analyse des données, 5(3), 283–310.

    Google Scholar 

  6. Bocca, B., Alimonti, A., Senofonte, O., Pino, A., Violante, N., Petrucci, F., et al. (2006). Metal changes in CSF and peripheral compartments of parkinsonian patients. Journal of the Neurological Sciences, 248(1), 23–30.

    CAS  Article  Google Scholar 

  7. Bressler, J. P., Olivi, L., Cheong, J. H., Kim, Y., Maerten, A., & Bannon, D. (2007). Metal transporters in intestine and brain: Their involvement in metal-associated neurotoxicities. Human and Experimental Toxicology, 26, 221–229.

    CAS  Article  Google Scholar 

  8. Breydo, L., & Uversky, V. N. (2011). Role of metal ions in aggregation of intrinsically disordered proteins in neurodegenerative diseases. Metallomics, 3(11), 1163–1180.

    CAS  Article  Google Scholar 

  9. Cabral Pinto, M. M. S., Almeida, A., Pinto, E., Freitas, S., Simões, M., Diniz, L., et al. (2015). Occupational and environmental exposure to Mn in manganese mining areas (South Portugal) and the occurrence of dementia. In 25th Alzheimer Europe Conference “Dementia: Putting strategies and research into practice”.

  10. Cabral Pinto, M. M. S., Freitas, S., Simões, M., Moreira, P. I., Dinis, L., & Ferreira da Silva, E. A. (2013). Neurodegenerative diseases in the Estarreja (Central Portugal) inhabitants and their potential relationship with trace elements in the environment—preliminary results. In 5th International conference on medical geology, 25–29 Aug, 2013, Virginia.

  11. Cachada, A., Pereira, M. E., Ferreira da Silva, E., & Duarte, A. C. (2012). Sources of potentially toxic elements and organic pollutants in an urban area subjected to an indus-trial impact. Environmental Monitoring and Assessment, 184, 15–32.

    CAS  Article  Google Scholar 

  12. Cerpa, W., Varela-Nallar, L., Reyes, A. E., Minniti, A. N., & Inestrosa, C. (2005). Is there a role for copper in neurodegenerativediseases? Molecular Aspects of Medicine, 26, 405–420.

    CAS  Article  Google Scholar 

  13. Chin-Chan, M., Navarro-Yepes, J., & Quintanilla-Vega, B. (2015). Environmental pollutants as risk factors for neurodegenerative disorders: Alzheimer and Parkinson diseases. Frontiers in Cellular Neuroscience, 9, 124.

    Article  CAS  Google Scholar 

  14. Coelho, P., Costa, S., Silva, S., Walter, A., Ranville, J., Sousa, A. C., et al. (2012). Metal (loid) levels in biological matrices from human populations exposed to mining contamination—Panasqueira Mine (Portugal). Journal of Toxicology and Environmental Health, 75, 893–908.

    CAS  Article  Google Scholar 

  15. Condesso de Melo, M. T., & Marques da Silva, M. A. (2008). The aveiro quaternary and cretaceous aquifers. In W. M. Edmunds & P. Shand (Eds.), The natural baseline quality of groundwater. Oxford: Blackwell Publishers.

    Google Scholar 

  16. Costa, C., & Jesus-Rydin, C. (2001). Site investigation on heavy metals contaminated ground in Estarreja—Portugal. Engineering Geology, 60, 39–47.

    Article  Google Scholar 

  17. Dorne, J. L., Kass, G. E., Bordajandi, L. R., Amzal, B., Bertelsen, U., Castoldi, A. F., et al. (2011). Human risk assessment of heavy metals: Principles and applications. Metal Ions in Life Sciences, 8, 27–60.

    CAS  Google Scholar 

  18. Elsner, R. J., & Spangler, J. G. (2005). Neurotoxicity of inhaled manganese: Public health danger in the shower? Medical Hypotheses, 65(3), 607–616.

    CAS  Article  Google Scholar 

  19. Ericson, I., Martí-Cid, R., Nadal, M., Van Bavel, B., Lindström, G., & Domingo, J. L. (2008). Human exposure to perfluorinated chemicals through the diet: Intake of perfluorinated compounds in foods from the Catalan (Spain) market. Journal of Agricultural and Food Chemistry, 56(5), 1787–1794.

    CAS  Article  Google Scholar 

  20. Exley, C. (2012). The coordination chemistry of aluminium in neurodegenerative disease. Coordination Chemistry Reviews, 256(19), 2142–2146.

    CAS  Article  Google Scholar 

  21. Exley, C., & House, E. R. (2012). Aluminium in the human brain (pp. 95–101). Vienna: Springer.

    Google Scholar 

  22. Fabrizio, E., Vanacore, N., Valente, M., Rubino, A., & Meco, G. (2007). High prevalence of extrapyramidal signs and symptoms in a group of Italian dental technicians. BMC Neurology, 3, 7–24.

    Google Scholar 

  23. Ferrer, I. (2012). Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia. Progress in Neurobiology, 97(1), 38–51.

    Article  Google Scholar 

  24. Folstein, M., Folstein, S., & McHugh, P. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.

    CAS  Article  Google Scholar 

  25. Forte, G., Bocca, B., Senofonte, O., Petrucci, F., Brusa, L., Stanzione, P., et al. (2004). Trace and major elements in whole blood, serum, cerebrospinal fluid and urine of patients with Parkinson’s disease. Journal of Neural Transmission, 111(8), 1031–1040.

    CAS  Article  Google Scholar 

  26. Forte, G., Deiana, M., Pasella, S., Baralla, A., Occhineri, P., Mura, I., et al. (2014). Metals in plasma of nonagenarians and centenarians living in a key area of longevity. Experimental Gerontology, 60, 197–206.

    CAS  Article  Google Scholar 

  27. Freitas, S., Simões, M. R., Alves, L., & Santana, I. (2011). Montreal Cognitive Assessment (MoCA): Normative study for the Portuguese population. Journal of Clinical and Experimental Neuropsychology, 33(9), 989–996.

    Article  Google Scholar 

  28. Freitas, S., Simões, M. R., Alves, L., & Santana, I. (2013). Montreal Cognitive Assessment (MoCA): Validation study for mild cognitive impairment and Alzheimer´s disease. Alzheimer Disease and Associated Disorders, 27(1), 37–43.

    Article  Google Scholar 

  29. Freitas, S., Simões, M. R., Alves, L., & Santana, I. (2015). The relevance of sociodemographic and health variables on MMSE normative data. Applied Neuropsychology: Adults, 22(4), 311–319.

    Article  Google Scholar 

  30. Gaenslen, A., Unmuth, B., Godau, J., Liepelt, I., Di Santo, A., Schweitzer, K. J., et al. (2008). The specificity and sensitivity of transcranial ultrasound in the differential diagnosis of Parkinson’s disease: A prospective blinded study. The Lancet Neurology, 7(5), 417–424.

    Article  Google Scholar 

  31. Ganrot, P. O. (1986). Metabolism and possible health effects of aluminum. Environmental Health Perspectives, 65, 363.

    CAS  Google Scholar 

  32. Garret, C., Santos, F., Tracana, I., Barreto, J., Sobral, M., & Fonseca, R. (2008). Avaliação Clínica da Demência (Clinical Dementia Rating Scale). In Grupo de Estudos de Envelhecimento Cerebral e Demências (Study Group on Brain Aging and Dementia) (Ed.), Escalas e testes na demência (Scales and tests in dementia) (pp. 17–32). Lisbon: GEECD.

    Google Scholar 

  33. Goldberg, D. P., Gater, R., Sartorius, N., Ustun, T., Piccinelli, M., Gureje, O., et al. (1997). The validity of two versions of the GHQ in the WHO study of mental illness in general health care. Psychological Medicine, 27(01), 191–197.

    CAS  Article  Google Scholar 

  34. Gomes, C. M., & Wittung-Stafshede, P. (Eds.). (2010). Protein folding and metal ions: Mechanisms, biology and disease. Boca Raton: CRC Press.

    Google Scholar 

  35. Gorell, J. M., Johnson, C. C., Rybicki, B. A., Peterson, E. L., Kortsha, G. X., Kortsha, G. G., et al. (1999). Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson’s disease. Neurotoxicology, 20, 239–248.

    CAS  Google Scholar 

  36. Goullé, J. P., Mahieu, L., Castermant, J., Neveu, N., Bonneau, L., Lainé, G., et al. (2005). Metal and metalloid multi-elementary ICP-MS validation in whole blood, plasma, urine and hair: Reference values. Forensic Science International, 153(1), 39–44.

    Article  CAS  Google Scholar 

  37. Greenacre, M. J. (1984). Theory and applications of correspondence analysis. London: Academic Press.

  38. Gupta, V. B., Anitha, S., Hegde, M. L., Zecca, L., Garruto, R. M., Ravid, R., et al. (2005). Aluminium in Alzheimer’s disease: Are we still at a crossroad? Cellular and Molecular Life Sciences CMLS, 62(2), 143–158.

    CAS  Article  Google Scholar 

  39. Hao, Z., Li, Y., Liu, Y., Li, H., Wang, W., & Yu, J. (2015). Hair elements and healthy aging: A cross-sectional study in Hainan Island, China. Environmental Geochemistry and Health, 38(3), 723–735. doi:10.1007/s10653-015-9755-3.

    CAS  Article  Google Scholar 

  40. Hozumi, I., Hasegawa, T., Honda, A., Ozawa, K., Hayashi, Y., Hashimoto, K., et al. (2011). Patterns of levels of biological metals in CSF differ among neurodegenerative diseases. Journal of the Neurological Sciences, 303(1), 95–99.

    CAS  Article  Google Scholar 

  41. Hughes, C. P., Berg, L., Danziger, W. L., Coben, L. A., & Martin, R. L. (1982). A new clinical scale for the staging of dementia. The British Journal of Psychiatry, 140, 566–572.

    CAS  Article  Google Scholar 

  42. Inácio, M., Neves, O., Pereira, V., & da Silva, E. F. (2014). Levels of selected potential harmful elements (PHEs) in soils and vegetables used in diet of the population living in the surroundings of the Estarreja Chemical Complex (Portugal). Applied Geochemistry, 44, 38–44.

    Article  CAS  Google Scholar 

  43. INE. (2012). CENSUS 2001. http://censos.ine.pt/xportal/xmain?xpid=CENSOS&xpgid=censos_quadros_populacao.

  44. Johnson, F. O., & Atchison, W. D. (2009). The role of environmental mercury, lead and pesticide exposure in development of amyotrophic lateral sclerosis. NeuroToxicology, 30(5), 761–765.

    CAS  Article  Google Scholar 

  45. Karagas, M. R., Stukel, T. A., Morris, J. S., Tosteson, T. D., Weiss, J. E., Spencer, S. K., et al. (2001). Skin cancer risk in relation to toenail arsenic concentrations in a US population-based case-control study. American Journal of Epidemiology, 153(6), 559–565.

    CAS  Article  Google Scholar 

  46. Kasper-Sonnenberg, M., Sugiri, D., Wurzler, S., Ranft, U., Dickel, H., Wittsiepe, J., et al. (2011). Prevalence of nickel sensitization and urinary nickel content of children are increased by nickel in ambient air. Environmental Research, 111(2), 266–273.

    CAS  Article  Google Scholar 

  47. Kazi, T. G., Afridi, H. I., Kazi, N., Jamali, M. K., Arain, M. B., Jalbani, N., et al. (2008). Copper, chromium, manganese, iron, nickel, and zinc levels in biological samples of diabetes mellitus patients. Biological Trace Element Research, 122(1), 1–18.

    CAS  Article  Google Scholar 

  48. Komatina, M. M. (2004). Medical geology—Effects of geological environments on human health. Developments in Earth & Environmental Sciences (Vol. 2). Amsterdam: Elsevier.

    Google Scholar 

  49. Kozlowski, H., Janicka Klosb, A., Brasunb, J., Gaggelli, E., Valensinc, D., & Valensinc, J. (2009). Copper, iron, and zinc ions homeostasis and their role in neurodegenerative disorders (metal uptake, transport, distribution and regulation). Coordination Chemistry Reviews, 253, 2665–2685.

    CAS  Article  Google Scholar 

  50. Kuiper, N., Rowell, C., Nriagu, J., & Shomar, B. (2014). What do the trace metal contents of urine and toenail samples from Qatar’s farm workers bioindicate? Environmental Research, 131, 86–94.

    CAS  Article  Google Scholar 

  51. Leitão, T. B. E. (1996). Metodologia para a reabilitação de aquíferos poluídos. Ph.D. Thesis. Faculdade de Ciências da Universidade de Lisboa.

  52. Lemos, R., Duro, D., Simões, M. R., & Santana, I. (2014). The free and cued selective reminding test distinguishes frontotemporal dementia from Alzheimer’s disease. Archives of Clinical Neuropsychology, 29(7), 670–679.

    Article  Google Scholar 

  53. Liu, C. P., Luo, C. L., Gao, Y., Li, F. B., Lin, L. W., Wu, C. A., et al. (2010). Arsenic contamination and potential health risk implications at an abandoned tungsten mine, southern China. Environmental Pollution, 158(3), 820–826.

    CAS  Article  Google Scholar 

  54. Marchiset-Ferlay, N., Savanovitch, C., & Sauvant-Rochat, M. P. (2012). What is the best biomarker to assess arsenic exposure via drinking water? Environment International, 39(1), 150–171.

    CAS  Article  Google Scholar 

  55. Martyn, C. N., Osmond, C., Edwardson, J. A., Barker, D. J. P., Harris, E. C., & Lacey, R. F. (1989). Geographical relation between Alzheimer’s disease and aluminium in drinking water. The Lancet, 333(8629), 61–62.

    Article  Google Scholar 

  56. Maynard, C. J., Bush, A. I., Masters, C. L., Cappai, R., & Li, Q. X. (2005). Metals and amyloid-β in Alzheimer’s disease. International Journal of Experimental Pathology, 86(3), 147–159.

    CAS  Article  Google Scholar 

  57. Monnet-Tschudi, F., Zurich, M.-G., Boschat, C., Corbaz, A., & Honegger, P. (2006). Involvement of environmental mercury and lead in the etiology of neurodegenerative diseases. Reviews on Environmental Health Reviews on Environmental Health, 21(2), 105–118.

    CAS  Google Scholar 

  58. Moreira, P. I., Honda, K., Liu, Q., Santos, M. S., Oliveira, C. R., Aliev, G., et al. (2005). Oxidative stress: The old enemy in Alzheimer’s disease pathophysiology. Current Alzheimer Research, 2, 403–408.

    CAS  Article  Google Scholar 

  59. Moreira, P. I., Zhu, X., Lee, H.-G., Honda, K., Smith, M. A., & Perry, G. (2006). The (un)balance between metabolic and oxidative abnormalities and cellular compensatory responses in Alzheimer disease. Mechanisms of Ageing and Development, 127, 501–506.

    CAS  Article  Google Scholar 

  60. Morris, J. C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43, 2412–2414.

    CAS  Article  Google Scholar 

  61. Nasreddine, Z., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., et al. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. American Geriatrics Society, 53(4), 695–699.

    Article  Google Scholar 

  62. Ndilila, W., Callan, A. C., McGregor, L. A., Kalin, R. M., & Hinwood, A. L. (2014). Environmental and toenail metals concentrations in copper mining and non mining communities in Zambia. International Journal of Hygiene and Environmental Health, 217(1), 62–69.

    CAS  Article  Google Scholar 

  63. Nriagu, G. (2007). Zinc toxicity in humans (pp. 1–7). Elsevier. https://pdfs.semanticscholar.org/a9e2/8321ae506e646f32ce59d87b7589851aa7e4.pdf.

  64. Ordens, C. M. (2007). Estudo da contaminação do aquífero superior na região de Estarreja. Unpublished M.Sc. thesis. Coimbra University. http://www.lneg.pt/download/3268/carlos_ordens.pdf. Accessed 11 Mar 2015.

  65. Ordens, C. M., Condesso de Melo, M. T., Grangeia, C., & Marques da Silva, M. A. (2007). Groundwater–surface water interactions near a Chemical Complex (Estarreja, Portugal)—Implications on groundwater quality. In Proceedings 35th congress of international association of hydrogeologists, Lisbon, Portugal, 17–21 Sept.

  66. Pereira, M. E., Lillebø, A. I., Pato, P., Válega, M., Coelho, J. P., Lopes, C., et al. (2009). Mercury pollution in Ria de Aveiro (Portugal): A review of the system assessment. Environment Monitoring and Assessment, 155, 39–49.

    CAS  Article  Google Scholar 

  67. Perl, D. P., & Moalem, S. (2006). Aluminum and Alzheimer’s disease, a personal perspective after 25 years. Journal of Alzheimer’s Disease, 9(3), 291–300.

    CAS  Article  Google Scholar 

  68. Pocinho, M. T. S., Farate, C., Dias, C. A., Lee, T. T., & Yesavage, J. A. (2009). Clinical and psychometric validation of the Geriatric Depression Scale (GDS) for Portuguese Elders. Clinical Gerontologist, 32, 223–236.

    Article  Google Scholar 

  69. Polizzi, S., Pira, E., Ferrara, M., Bugiani, M., Papaleo, A., Albera, R., et al. (2002). Neurotoxic effects of aluminium among foundry workers and Alzheimer’s disease. Neurotoxicology, 23(6), 761–774.

    CAS  Article  Google Scholar 

  70. Portuguese Decree 236. (1998). Portuguese legislation on water quality. Diário da República IA (pp. 3676–3722). http://dre.pt/pdf1sdip/1998/08/176A00/36763722.pdf

  71. Portuguese Decree 306. (2007). Portuguese legislation on water quality. Diário da República IA (pp. 5747–5765). http://dre.pt/pdf1sdip/2007/08/16400/0574705765.pdf

  72. Post, G. B., Cohn, P. D., & Cooper, K. R. (2012). Perfluorooctanoic acid (PFOA), an emerging drinking water contaminant: A critical review of recent literature. Environmental Research, 116, 93–117.

    CAS  Article  Google Scholar 

  73. Reis, A. P., Costa, S., Santos, I., Patinha, C., Noack, Y., Wragg, J., et al. (2015). Investigating relationships between biomarkers of exposure and environmental copper and manganese levels in house dusts from a Portuguese industrial city. Environmental Geochemistry and Health, 37(4), 725–744.

    CAS  Article  Google Scholar 

  74. Reis, A. P., Menezes de Almeida, L., Ferreira da Silva, E., Sousa, A. J., Patinha, C., & Fonseca, E. C. (2007). Assessing the geochemical inherent quality of natural soils in the Douro river basin for grapevine cultivation using data analysis and geostatistics. Geoderma, 141, 370–383.

    CAS  Article  Google Scholar 

  75. Reis, A. P., Patinha, C., Ferreira da Silva, E., Sousa, A., Figueira, R., Sérgio, C., et al. (2010). Assessment of human exposure to environmental heavy metals in soils and bryophytes of the central region of Portugal. International Journal of Environmental Health Research, 20(2), 87–113. doi:10.1080/09603120903394649.

    CAS  Article  Google Scholar 

  76. Reis, A. P., Sousa, A. J., Ferreira Da Silva, E., Patinha, C., & Fonseca, E. C. (2004). Combining multiple correspondence analysis with factorial kriging analysis for geochemical mapping of the gold-silver deposit at Marrancos (Portugal). Applied Geochemistry, 19(4), 623–631. doi:10.1016/j.apgeochem.2003.09.003.

    CAS  Article  Google Scholar 

  77. Roberts, N. B., Clough, A., Bellia, J. P., & Kim, J. Y. (1998). Increased absorption of aluminium from a normal dietary intake in dementia. Journal of Inorganic Biochemistry, 69(3), 171–176.

    CAS  Article  Google Scholar 

  78. Rodella, L. S., Ricci, F., Borsani, E., Stacchiotti, A., Foglio, E., Favero, G., et al. (2008). Aluminium exposure induces Alzheimer’ disease-like histopathological alterations in mouse brain. Histology and Histopathology, 23, 433–439.

    CAS  Google Scholar 

  79. Rogers, M. A., & Simon, D. G. (1999). A preliminary study of dietary aluminium intake and risk of Alzheimer’s disease. Age and Ageing, 28(2), 205–209.

    CAS  Article  Google Scholar 

  80. Santana, I., Vicente, M., Freitas, S., Santiago, B., & Simões, M. R. (2015). Avaliação Clínica da Demência (CDR) (Clinic Dementia Rating, CDR). In Mário R. Simões, Isabel Santana e Grupo de Estudos de Envelhecimento Cerebral e Demência (Eds.), Escalas e Testes na Demência (3ª. edição, pp. 12–17) (Scales and tests in dementia, 3rd edn.). Lisboa: Novartis.

  81. Simões, M. R., Freitas, S., Santana, I., Firmino, H., Martins, C., Nasreddine, Z., et al. (2008). Montreal Cognitive Assessment (MoCA): Versão portuguesa (Montreal Cognitive Assessment (MoCA): Portuguese version). Coimbra: Serviço de Avaliação Psicológica da Faculdade de Psicologia e de Ciências da Educação da Universidade de Coimbra (Psychological Assessment Department, Faculty of Psychology and Educational Sciences, University of Coimbra).

    Google Scholar 

  82. Simões, M. R., Prieto, G., Pinho, M. S., & Firmino, H. (2015). Geriatric Depression Scale (GDS-30). In Mário R. Simões, Isabel Santana e Grupo de Estudos de Envelhecimento Cerebral e Demência (Eds.), Escalas e Testes na Demência (3ª. edição, pp. 128–133) (Scales and tests in dementia, 3rd edn.). Lisboa: Novartis.

  83. Tartaglione, A. M., Venerosi, A., & Calamandrei, G. (2015). Early-life toxic insults and onset of sporadic neurodegenerative diseases—an overview of experimental studies. In Neurotoxin Modeling of Brain Disorders—Life-long Outcomes in Behavioral Teratology (pp. 231–264). Springer International Publishing.

  84. Teixeira, C., & Assunção, C. F. T. (1963). Over geological map, 13C. Lisboa: Instituto Geográfico e Cadastral.

    Google Scholar 

  85. Van der Voet, G. B. (1992). Intestinal absorption of aluminum. In Isaacson, R. L., & Jensen, K. F. (Eds.), The vulnerable brain and environmental risks (pp. 35–47). Plenum Press, Springer US.

  86. Van der Weijden, C., & Pacheco, F. A. L. (2006). Hydrogeochemistry in the Vouga River basin (central Portuhal): Pollution and chemical weathering. Applied Geochemistry, 21, 580–613.

    Article  CAS  Google Scholar 

  87. Viaene, M. K., Masschelein, R., Leenders, J., De Groof, M., Swerts, L. J., Roels, H., et al. (2000). Neurobehavioural effects of occupational exposure to cadmium: A cross sectional epidemiological study. Occupational and Environmental Medicine, 57, 19–27.

    CAS  Article  Google Scholar 

  88. Wang, B., & Du, Y. (2013). Review article cadmium and its neurotoxic effects. Oxidative Medicine and Cellular Longevity. doi:10.1155/2013/898034.

    Article  Google Scholar 

  89. World Health Organisation. (2011). Guidelines for drinking-water quality (4th ed). http://who.int/en/. 28 Apr 2016.

  90. Yegambaram, M., Manivannan, B., Beach, T. G., & Halden, R. U. (2015). Role of environmental contaminants in the etiology of Alzheimer’s disease: A review. Current Alzheimer Research, 12(2), 116–146.

    CAS  Article  Google Scholar 

  91. Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Huang, V., Adey, M., et al. (1983). Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatric Research, 17(1), 37–49.

    CAS  Article  Google Scholar 

  92. Yokel, R. A. (2006). Blood-brain barrier flux of aluminum, manganese, iron and other metals suspected to contribute to metal-induced neurodegeneration. Journal of Alzheimer’s Disease, 10(2–3), 223–253.

    Article  Google Scholar 

  93. Zatta, P., Lucchini, R., Van Rensburg, S. J., & Taylor, A. (2003). The role of metals in neurodegenerative processes: Aluminum, manganese, and zinc. Brain Research Bulletin, 62, 15–28.

    CAS  Article  Google Scholar 

  94. Zhang, B., Cheng, X. R., da Silva, I. S., Hung, V. W., Veloso, A. J., Angnes, L., et al. (2013). Electroanalysis of the interaction between (−)-epigallocatechin-3-gallate (EGCG) and amyloid-β in the presence of copper. Metallomics, 5(3), 259–264.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Funding for this research was provided by the Labex DRIIHM, Réseau des Observatoires Hommes-Millieux–Centre National de la Recherche Scientifique (ROHM–CNRS) and OHM.I-Estarreja and by the Foundation for Science and the Technology (SFRH/BPD/71030/2010 and the Projects UI/D/GEO/04035/2013 and UID/MAR/04292/2013). We thank the participants for taking part in this research and the local private institutions of social solidarity for the collaboration (Santa Casa Misericórdia de Estarreja, Associação Humanitária de Salreu, Centro Paroquial Social São Tomé de Canelas, Centro Paroquial Social Avanca, Fundação Cónego Filipe Figueiredo Beduíno, Centro Paroquial de Pardilhó). The authors are grateful to Eugénio Soares from the Central Laboratory of University of Aveiro. The manuscript benefited from careful and constructive reviews by Shweta Modgil and two anonymous reviewers.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marina M. S. Cabral Pinto.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 14 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cabral Pinto, M.M.S., Marinho-Reis, A.P., Almeida, A. et al. Human predisposition to cognitive impairment and its relation with environmental exposure to potentially toxic elements. Environ Geochem Health 40, 1767–1784 (2018). https://doi.org/10.1007/s10653-017-9928-3

Download citation

Keywords

  • Neurodegenerative diseases
  • Environmental exposure
  • Potentially toxic elements
  • Urine
  • Groundwater