Associations between Trace Elements and Cognitive Decline: An Exploratory 5-Year Follow-Up Study of an Elderly Cohort
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants and Study Design
2.2. Geographical Areas of Interest
2.3. Neuropsychological Assessment
- The Mini Mental State Examination (MMSE [49,50]), which is a brief cognitive screening tool widely used in the assessment of cognitive impairment [53]. It is composed of 30 dichotomous items (0—incorrect; 1—correct) and assesses 5 cognitive domains: Orientation, Memory, Attention and Calculus, Language, and Visuoconstruction. Higher scores indicate better cognitive performance.
- The Montreal Cognitive Assessment (MoCA [51,52]), which is a screening tool developed to detect milder forms of cognitive decline, such as Mild Cognitive Impairment (MCI [67]). This instrument assesses 6 cognitive domains—Executive Functions; Visuospatial Abilities; Memory; Language; Attention Concentration and Working Memory; Temporal and Spatial Orientation—on a scale of 30 points, whose higher global scores translate better cognitive functioning.
- The Geriatric Depression Scale—30 (GDS-30 [46,47,48]), which is a brief scale specifically developed for the screening of depressive symptoms in advanced adulthood. It is composed of 30 yes/no questions regarding the affective and cognitive domains of depression. Greater scores indicate more severe symptomatology.
2.4. Fingernail Samples and Analysis
2.5. Statistical Analysis
3. Results
3.1. Sample Characterization
3.2. Neuropsychological Data
3.3. TE Content in Fingernails
3.4. Relationship between Fingernail TE Content and Cognitive Performance
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- WHO. Global Health and Aging. Available online: https://www.who.int/ageing/publications/global_health.pdf (accessed on 9 March 2020).
- OECD. Health at a Glance 2019. Available online: https://www.oecd-ilibrary.org/social-issues-migration-health/health-at-a-glance-2019_4dd50c09-en (accessed on 9 March 2020).
- Statistics Portugal. Censos 2011, XV Recenseamento Geral da População, V Recenseamento Geral da Habitação, Resultados Definitivos, Portugal [2011 Census, XV General Population Census, V General Housing Census, Definitive Results, Portugal]; INE: Lisbon, Portugal, 2015; ISBN 978-989-25-0181-9.
- Wimo, A.; Guerchet, M.; Ali, G.C.; Wu, Y.T.; Prina, A.M.; Winblad, B.; Jönsson, L.; Liu, Z.; Prince, M. The worldwide costs of dementia 2015 and comparisons with 2010. Alzheimers Dement. 2017, 13, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Tartaglione, A.M.; Venerosi, A.; Calamandrei, G. 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; Kostrzewa, R.M., Archer, T., Eds.; Springer: Cham, Switzerland; Boston, MA, USA, 2015; Volume 29, pp. 231–264. ISBN 978-3-319-34136-1. [Google Scholar]
- Yan, D.; Zhang, Y.; Liu, L.; Yan, H. Pesticide exposure and risk of Alzheimer’s disease: A systematic review and meta-analysis. Sci. Rep. 2016, 6, 32222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paglia, G.; Miedico, O.; Cristofano, A.; Vitale, M.; Angiolillo, A.; Chiaravalle, A.E.; Corso, G.; Di Costanzo, A. Distinctive pattern of serum elements during the progression of Alzheimer’s disease. Sci. Rep. 2016, 6, 22769. [Google Scholar] [CrossRef] [PubMed]
- Perl, D.P. Neuropathology of Alzheimer’s disease. Mt. Sinai J. Med. 2010, 77, 32–42. [Google Scholar] [CrossRef] [PubMed]
- Dourlen, P.; Kilinc, D.; Malmanche, N.; Chapuis, J.; Lambert, J.C. The new genetic landscape of Alzheimer’s disease: From amyloid cascade to genetically driven synaptic failure hypothesis? Acta Neuropathol. 2019, 138, 221–226. [Google Scholar] [CrossRef] [Green Version]
- Yegambaram, M.; Manivannan, B.; Beach, T.G.; Halden, R.U. Role of environmental contaminants in the etiology of Alzheimer’s disease: A review. Curr. Alzheimer Res. 2015, 12, 116–146. [Google Scholar] [CrossRef]
- Killin, L.O.; Starr, J.M.; Shiue, I.J.; Russ, T.C. Environmental risk factors for dementia: A systematic review. BMC Geriatr. 2016, 16, 1–28. [Google Scholar] [CrossRef] [Green Version]
- McAllum, E.J.; Finkelstein, D.I. Metals in Alzheimer’s and Parkinson’s disease: Relevance to dementia with lewy bodies. J. Mol. Neurosci. 2016, 60, 279–288. [Google Scholar] [CrossRef]
- Ayton, S.; Lei, P.; Bush, A.I. Metallostasis in Alzheimer’s disease. Free Radic. Biol. Med. 2013, 62, 76–89. [Google Scholar] [CrossRef]
- Gupta, V.B.; Anitha, S.; Hegde, M.L.; Zecca, L.; Garruto, R.M.; Ravid, R.; Shankar, S.K.; Stein, R.; Shanmugavelu, P.; Rao, K.J. Aluminium in Alzheimer’s disease: Are we still at a crossroad? Cell Mol. Life Sci. 2005, 62, 143–158. [Google Scholar] [CrossRef]
- Lucaroni, F.; Ambrosone, C.; Paradiso, F.; Messinese, M.; Di Domenicantonio, R.; Alessandroni, C.; Cicero, C.E.; Cerutti, F.; Di Gaspare, F.; Morciano, L.; et al. Metals Dyshomeostasis in Alzheimer’s Disease: A Systematic Review. Biomed. Prev. 2017, 2, 112. [Google Scholar] [CrossRef]
- Cicero, C.E.; Mostile, G.; Vasta, R.; Rapisarda, V.; Santo Signorelli, S.; Ferrante, M.; Zappia, M.; Nicoletti, A. Metals and neurodegenerative diseases. A systematic review. Environ. Res. 2017, 159, 82–94. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, P.C.; Tonani, K.A.; Julião, F.C.; Cupo, P.; Domingo, J.L.; Segura-Muñoz, S.I. Aluminum concentrations in water of elderly people’s houses and retirement homes and its relation with elderly health. Bull. Environ. Contam. Toxicol. 2009, 83, 565–569. [Google Scholar] [CrossRef] [PubMed]
- Zapatero, M.D.; Garcia de Jalon, A.; Pascual, F.; Calvo, M.L.; Escanero, J.; Marro, A. Serum aluminum levels in Alzheimer’s disease and other senile dementias. Biol. Trace Elem. Res. 1995, 47, 235–240. [Google Scholar] [CrossRef] [PubMed]
- Smorgon, C.; Mari, E.; Atti, A.R.; Dalla Nora, E.; Zamboni, P.F.; Calzoni, F.; Passaro, A.; Fellin, R. Trace elements and cognitive impairment: An elderly cohort study. Arch. Gerontol. Geriatr. 2004, 9, 393–402. [Google Scholar] [CrossRef] [PubMed]
- González-Domínguez, R.; García-Barrera, T.; Gómez-Ariza, J.L. Characterization of metal profiles in serum during the progression of Alzheimer’s disease. Metallomics 2014, 6, 292–300. [Google Scholar] [CrossRef]
- Graham, S.F.; Nasaruddin, M.B.; Carey, M.; Holscher, C.; McGuinness, B.; Kehoe, P.G.; Love, S.; Passmore, P.; Elliott, C.T.; Meharg, A.A.; et al. Age-Associated changes of brain copper, iron and zinc in alzheimer’s disease and dementia with lewy bodies. J. Alzheimers Dis. 2014, 42, 1407–1413. [Google Scholar] [CrossRef]
- Rembach, A.; Doecke, J.D.; Roberts, B.R.; Watt, A.D.; Faux, N.G.; Volitakis, I.; Pertile, K.K.; Rumble, R.L.; Trounson, B.O.; Fowler, C.J.; et al. Longitudinal analysis of serum copper and ceruloplasmin in Alzheimer’s disease. J. Alzheimers Dis. 2013, 34, 171–182. [Google Scholar] [CrossRef] [Green Version]
- Akatsu, H.; Hori, A.; Yamamoto, T.; Yoshida, M.; Mimuro, M.; Hashizume, Y.; Tooyama, I.; Yezdimer, E.M. Transition metal abnormalities in progressive dementias. Biometals 2012, 25, 337–350. [Google Scholar] [CrossRef]
- Magaki, S.; Raghavan, R.; Mueller, C.; Oberg, K.C.; Vinters, H.V.; Kirsch, W.M. Iron, copper, and iron regulatory protein 2 in alzheimer’s disease and related dementias. Neurosci. Lett. 2007, 418, 72–76. [Google Scholar] [CrossRef] [Green Version]
- Xu, J.; Begley, P.; Church, S.J.; Patassini, S.; McHarg, S.; Kureishy, N.; Hollywood, K.A.; Waldvogel, H.J.; Liu, H.; Zhang, S.; et al. Elevation of brain glucose and polyol-pathway intermediates with accompanying brain-copper deficiency in patients with alzheimer’s disease: Metabolic basis for dementia. Sci. Rep. 2016, 6, 27524. [Google Scholar] [CrossRef] [PubMed]
- Smith, M.A.; Zhu, X.; Tabaton, M.; Liu, G.; McKeel Jr, D.W.; Cohen, M.L.; Wang, X.; Siedlak, S.L.; Dwyer, B.E.; Hayashi, T.; et al. Increased iron and free radical generation in preclinical Alzheimer disease and mild cognitive impairment. J. Alzheimers Dis. 2010, 19, 363–372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szabo, S.T.; Harry, G.J.; Hayden, K.M.; Szabo, D.T.; Birnbaum, L. Comparison of metal levels between postmortem brain and ventricular fluid in alzheimer’s disease and nondemented elderly controls. Toxicol. Sci. 2015, 150, 292–300. [Google Scholar] [CrossRef] [PubMed]
- Emard, J.F.; Andre, P.; Thouez, J.P.; Mathieu, J.; Boily, C.; Beaudry, M.; Cholette, A.; Robitaille, Y.; Bouchard, R.; Daoud, N.; et al. Geographical distribution of Alzheimer’s disease cases at birth and the geochemical profile of Saguenay-lac-Saint-Jean/Québec, Canada (image project). Water Air Soil Pollut. 1994, 72, 251–264. [Google Scholar] [CrossRef]
- Shen, X.L.; Yu, J.H.; Zhang, D.F.; Xie, J.X.; Jiang, H. Positive relationship between mortality from Alzheimer’s disease and soil metal concentration in mainland China. J. Alzheimers Dis. 2014, 42, 893–900. [Google Scholar] [CrossRef] [PubMed]
- Jomova, K.; Valko, M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283, 65–87. [Google Scholar] [CrossRef]
- Barnham, K.J.; Bush, A.I. Metals in Alzheimer’s and Parkinson’s diseases. Curr. Opin. Chem. Biol. 2008, 12, 222–228. [Google Scholar] [CrossRef]
- Mohmand, J.; Eqani, S.A.M.A.S.; Fasola, M.; Alamdar, A.; Mustafa, I.; Ali, N.; Liu, L.; Peng, S.; Shen, H. Human exposure to toxic metals via contaminated dust: Bio-accumulation trends and their potential risk estimation. Chemosphere 2015, 132, 142–151. [Google Scholar] [CrossRef]
- Antoniadis, V.; Shaheen, S.M.; Boersch, J.; Frohne, T.; Du Laing, G.; Rinklebe, J. Bioavailability and risk assessment of potentially toxic elements in garden edible vegetables and soils around a highly contaminated former mining area in Germany. J. Environ. Manag. 2017, 186, 192–200. [Google Scholar] [CrossRef]
- Cabral Pinto, M.M.S.; Marinho-Reis, P.; Almeida, A.; Pinto, E.; Neves, O.; Inácio, M.; Gerardo, B.; Freitas, S.; Simões, M.R.; Dinis, P.A.; et al. Links between cognitive status and trace element levels in hair for an environmentally exposed population: A case study in the surroundings of the estarreja industrial area. Int. J. Environ. Res. Public Health 2019, 16, 4560. [Google Scholar] [CrossRef] [Green Version]
- Cabral Pinto, M.M.S.; Marinho-Reis, A.P.; Almeida, A.; Ordens, C.M.; Silva, M.M.; Freitas, S.; Simões, M.R.; Moreira, P.I.; Dinis, P.A.; Diniz, M.L.; et al. Human predisposition to cognitive impairment and its relation with environmental exposure to potentially toxic elements. Environ. Geochem. Health 2018, 40, 1767–1784. [Google Scholar] [CrossRef] [PubMed]
- Júlvez, J.; Paus, T.; Bellinger, D.; Eskenazi, B.; Tiemeier, H.; Pearce, N.; Ritz, B.; White, T.; Ramchandani, P.; Gispert, J.D.; et al. Environment and brain development: Challenges in the global context. Neuroepidemiology 2016, 46, 79–82. [Google Scholar] [CrossRef] [Green Version]
- Genuis, S.J.; Kelln, K.L. Toxicant exposure and bioaccumulation: A common and potentially reversible cause of cognitive dysfunction and dementia. Behav. Neurol. 2015, 620143. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haut, M.W.; Hartzell, J.W.; Moram, M.T. Toxins in the Central Nervous System. In Textbook of Clinical Neuropsychology, 2nd ed.; Morgan, J.E., Ricker, J.H., Eds.; Routledge: New York, NY, USA, 2018; pp. 587–602. [Google Scholar]
- Singer, R. Neurotoxicity in Neuropsychology. In The Little Black Book of Neuropsychology: A Syndrome-Based Approach; Schoenberg, M.R., Scott, J.G., Eds.; Springer: New York, NY, USA, 2014; pp. 813–838. [Google Scholar]
- White, R.F.; Krengel, M.; Grashow, R. Neurotoxicology. In Clinical Neuropsychology: A Pocket Handbook for Assessment, 3rd ed.; Parsons, M.W., Hammeke, T.A., Eds.; American Psychological Association: Washington, DC, USA, 2014; pp. 338–362. [Google Scholar]
- He, K. Trace elements in nails as biomarkers in clinical research. Eur. J. Clin. Investig. 2011, 41, 98–102. [Google Scholar] [CrossRef]
- Clarkson, T.W.; Friberg, L.; Nordberg, G.F.; Sager, P.R. Biological Monitoring of Toxic Metals; Springer Science & Business Media: New York, NY, USA, 2012. [Google Scholar]
- Sureda, A.; Bibiloni, M.M.; Julibert, A.; Aparicio-Ugarriza, R.; Blé, G.P.L.; Pons, A.; Gonzalez-Gross, M.; Tur, J.A. Trace element contents in toenails are related to regular physical activity in older adults. PLoS ONE 2017, 12. [Google Scholar] [CrossRef] [Green Version]
- WHO. Human Biomonitoring: Facts and Figures. Available online: http://www.euro.who.int/__data/assets/pdf_file/0020/276311/Human-biomonitoring-facts-figures-en.pdf (accessed on 9 March 2020).
- Cabral-Pinto, M.M.; Inácio, M.; Neves, O.; Almeida, A.A.; Pinto, E.; Oliveiros, B.; da Silva, E.A.F. Human health risk assessment due to agricultural activities and crop consumption in the surroundings of an industrial area. Expos. Health 2019, 1–12. [Google Scholar] [CrossRef]
- Yesavage, J.A.; Brink, T.L.; Rose, T.L.; Lum, O.; Huang, V.; Adey, M.; Leirer, O. Development and validation of a geriatric depression screening scale: A preliminary report. J. Psychiatr Res. 1983, 17, 37–49. [Google Scholar] [CrossRef]
- Pocinho, M.T.S.; Farate, C.; Dias, C.A.; Lee, T.T.; Yesavage, J.A. Clinical and psychometric validation of the geriatric depression scale (GDS) for portuguese elders. Clin. Gerontol. 2009, 32, 223–236. [Google Scholar] [CrossRef]
- Simões, M.R.; Prieto, G.; Pinho, M.S.; Firmino, H. Geriatric Depression Scale (GDS-30). In Escalas e Testes na Demência [Scales and Tests in Dementia], 3rd ed.; Simões, M.R., Isabel Santana e Grupo de Estudos de Envelhecimento Cerebral e Demência, Eds.; Novartis: Lisboa, Portugal, 2015; pp. 128–133. [Google Scholar]
- Folstein, M.; Folstein, S.; McHugh, P. Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12, 189–198. [Google Scholar] [CrossRef]
- Guerreiro, M.; Silva, A.P.; Botelho, M.A.; Leitão, O.; Castro-Caldas, A.; Garcia, C. Adaptação à população portuguesa da tradução do “Mini Mental State Examination” (MMSE). Rev. Port. Neurol. 1994, 1, 9. [Google Scholar]
- Nasreddine, Z.S.; Phillips, N.A.; Bédirian, V.; Charbonneau, S.; Whitehead, V.; Collin, I.; Cummings, J.L.; Chertkow, H. The Montreal Cognitive Assessment, MoCA: A brief screening tool for Mild Cognitive Impairment. J. Am. Geriatr. Soc. 2005, 534, 695–699. [Google Scholar] [CrossRef] [PubMed]
- Simões, M.R.; Freitas, S.; Santana, I.; Firmino, H.; Martins, C.; Nasreddine, Z.; Vilar, M. Montreal Cognitive Assessment (MoCA): Versão Portuguesa [Montreal Cognitive Assessment (MoCA): Portuguese Version]; Serviço de Avaliação Psicológica da Faculdade de Psicologia e de Ciências da Educação da Universidade de Coimbra: Coimbra, Portugal, 2008. [Google Scholar]
- Freitas, S.; Simões, M.R.; Alves, L.; Santana, I. The relevance of sociodemographic and health variables on MMSE normative data. Appl. Neuropsychol. Adult 2015, 22, 311–319. [Google Scholar] [CrossRef] [PubMed]
- Freitas, S.; Simões, M.R.; Alves, L.; Santana, I. Montreal cognitive assessment: Influence of sociodemographic and health variables. Arch. Clin. Neuropsychol. 2012, 27, 165–175. [Google Scholar] [CrossRef] [PubMed]
- Anderson, T.M.; Sachdev, P.S.; Brodaty, H.; Trollor, J.; Andrews, G. Effects of sociodemographic and health variables on minimental state exam scores in older Australians. Am. J. Geriatr. Psychiatry 2007, 15, 467–476. [Google Scholar] [CrossRef]
- Bravo, G.; Hébert, R. Age and education specific reference values for the mini-mental and modified mini-mental state examination derived from a non-demented elderly population. Int. J. Geriatr. Psychiatry 1997, 12, 1008–1018. [Google Scholar] [CrossRef]
- Matallana, D.; Santacruz, C.; Cano, C.; Reyes, P.; Samper-Ternent, R.; Markides, K.S.; Ottenbacher, K.J.; Reyes-Ortiz, C.A. The relationship between educational level and Mini-Mental State Examination domains among older Mexican Americans. J. Geriatr. Psych. Neur. 2011, 24, 9–18. [Google Scholar] [CrossRef]
- Costa, C.; Jesus-Rydin, C. Site investigation on heavy metals contaminated ground in Estarreja—Portugal. Eng. Geol. 2001, 60, 39–47. [Google Scholar] [CrossRef]
- Inácio, M.; Neves, O.; Pereira, V.; da Silva, E.F. 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). J. Appl. Geochem. 2014, 44, 38–44. [Google Scholar] [CrossRef]
- Patinha, C.; Reis, A.P.; Dias, A.C.; Abduljelil, A.A.; Noack, Y.; Robert, S.; Cave, M.; da Silva, E.F. The mobility and human oral bioaccessibility of Zn and Pb in urban dusts of Estarreja (N Portugal). Environ. Geochem. Health 2015, 37, 115–131. [Google Scholar] [CrossRef]
- Leitão, T.B.E. Metodologia Para A Reabilitação De Aquíferos Poluídos. Ph.D. Thesis, University of Lisbon, Lisbon, Portugal, 1996. [Google Scholar]
- Van der Weijden, C.; Pacheco, F.A.L. Hydrogeochemistry in the Vouga River basin (central Portugal): Pollution and chemical weathering. J. Appl. Geochem. 2006, 21, 580–613. [Google Scholar] [CrossRef]
- Ordens, C.M. Estudo Da Contaminacão Do Aquífero Superior Na Região De Estarreja. Master’s Thesis, University of Coimbra, Coimbra, Portugal, 2007. [Google Scholar]
- Abreu, M.M.; Tavares, M.T.; Batista, M.J. Potential use of Erica andevalensis and Erica australis in phytoremediation of sulphide mine environments: São Domingos, Portugal. J. Geochem. Explor. 2008, 96, 210–222. [Google Scholar] [CrossRef] [Green Version]
- Oliveira, J.S.; Farinha, J.; Matos, J.X.; Ávila, P.; Rosa, C.; Machado, M.J.C.; Daniel, F.S.; Martins, L.; Leite, M.R.M. Diagnóstico ambiental das principais áreas mineiras degradadas do país [Environmental diagnosis of the main degraded mining areas of the country]. Boletim Minas 2002, 39, 67–85. [Google Scholar]
- Pérez-López, R.; Álvarez-Valero, A.M.; Nieto, J.M.; Sáez, R.; Matos, J.X. Use of sequential extraction procedure for assessing the environmental impact at regional scale of the São Domingos Mine (Iberian Pyrite Belt). Appl. Geochem. 2008, 23, 3452–3463. [Google Scholar] [CrossRef]
- Freitas, S.; Simões, M.R.; Alves, L.; Santana, I. Montreal Cognitive Assessment (MoCA): Normative study for the Portuguese population. J. Clin. Exp. Neuropsychol. 2011, 33, 989–996. [Google Scholar] [CrossRef]
- Bass, D.A.; Hickok, D.; Quig, D.; Urek, K. Trace element analysis in hair: Factors determining accuracy, precision, and reliability. Altern Med. Rev. 2001, 6, 472–481. [Google Scholar]
- IBM Corp. IBM SPSS Statistics for Windows; Version 22.0; IBM Corp: Armonk, NY, USA, 2013. [Google Scholar]
- Freitas, S.; Simões, M.R.; Alves, L.; Santana, I. Mini Mental State Examination (MMSE): Normative study for the Portuguese population in a community stratified sample. Appl. Neuropsychol. Adult 2015, 22, 311–319. [Google Scholar] [CrossRef]
- Freitas, S.; Simões, M.R.; Alves, L.; Santana, I. Montreal cognitive assessment: Validation study for mild cognitive impairment and Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2013, 27, 37–43. [Google Scholar] [CrossRef]
- Freitas, S.; Simões, M.R.; Alves, L.; Duro, D.; Santana, I. Montreal Cognitive Assessment (MoCA): Validation study for frontotemporal dementia. J. Geriatr. Psychiatry Neurol. 2012, 25, 146–154. [Google Scholar] [CrossRef]
- Freitas, S.; Simões, M.R.; Alves, L.; Vicente, M.; Santana, I. Montreal Cognitive Assessment (MoCA): Validation study for vascular dementia. J. Int. Neuropsychol. Soc. 2012, 18, 1031–1040. [Google Scholar] [CrossRef] [Green Version]
- Rodushkin, I.; Axelsson, M.D. Application of double focusing sector field ICP-MS for multielemental characterization of human hair and nails. Part II. A study of the inhabitants of northern Sweden. Sci. Total Environ. 2000, 262, 21–36. [Google Scholar] [CrossRef]
- Li, Y.; Zou, X.; Lv, J.; Yang, L.; Li, H.; Wang, W. Trace elements in fingernails of healthy chinese centenarians. Biol. Trace Elem. Res. 2012, 145, 158–165. [Google Scholar] [CrossRef] [PubMed]
- Cohen, J. Statistical Power Analysis for the Behavioural Sciences, 2nd ed.; Academic Press: New York, NY, USA, 1988. [Google Scholar]
- Cohen, J. A power primer. Psychol. Bull. 1992, 112, 155–159. [Google Scholar] [CrossRef] [PubMed]
- Moraes, C.; Pinto, J.A.; Lopes, M.A.; Litvoc, J.; Bottino, C.M. Impact of sociodemographic and health variables on mini-mental state examination in a community-based sample of older people. Eur. Arch. Psychiatry Clin. Neurosci. 2010, 260, 535–542. [Google Scholar] [CrossRef] [PubMed]
- Gonçalves-Pereira, M.; Cardoso, A.; Verdelho, A.; da Silva, J.A.; de Almeida, M.C.; Fernandes, A.; Raminhos, C.; Ferri, C.P.; Prina, M.; Prince, M. The prevalence of dementia in a Portuguese community sample: A 10/66 Dementia Research Group study. BMC Geriatr. 2017, 17, 261. [Google Scholar] [CrossRef] [PubMed]
- Hou, Y.; Dan, X.; Babbar, M.; Wei, Y.; Hasselbalch, S.G.; Croteau, D.L.; Bohr, V.A. Ageing as a risk factor for neurodegenerative disease. Nat. Rev. Neurol. 2019, 15, 565–581. [Google Scholar] [CrossRef]
- Larson, E.B.; Yaffe, K.; Langa, K.M. New insights into the dementia epidemic. N. Engl. J. Med. 2013, 369, 2275–2277. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Trivedi, A.V. A review on role of nickel in the biological system. Int. J. Curr. Microbiol. Appl. Sci. 2016, 5, 719–727. [Google Scholar] [CrossRef]
- Song, X.; Kenston, S.S.F.; Kong, L.; Zhao, J. Molecular mechanisms of nickel induced neurotoxicity and chemoprevention. Toxicology 2017, 392, 47–54. [Google Scholar] [CrossRef]
- Chen, Q.Y.; Brocato, J.; Laulicht, F.; Costa, M. Mechanisms of Nickel Carcinogenesis. In Essential and Non-Essential Metals. Molecular and Integrative Toxicology; Mudipalli, A., Zelikoff, J., Eds.; Springer International Publishing AG: New York, NY, USA, 2017; pp. 181–197. ISBN 978-3-319-55446-4. [Google Scholar]
- Zambelli, B.; Uversky, V.N.; Ciurli, S. Nickel impact on human health: An intrinsic disorder perspective. Biochim. Biophys. Acta Proteins Proteom. 2016, 1864, 1714–1731. [Google Scholar] [CrossRef]
- Poonkothai, M.; Vijayavathi, B.S. Nickel as an essential element and a toxicant. Int. J. Eng. Sci. Technol. 2012, 1, 285–288. [Google Scholar]
- Zhao, J.; Shi, X.; Castranova, V.; Ding, M. Occupational toxicology of nickel and nickel compounds. J. Environ. Pathol. Toxicol. Oncol. 2009, 28, 177–208. [Google Scholar] [CrossRef] [PubMed]
- Genchi, G.; Carocci, A.; Lauria, G.; Sinicropi, M.S.; Catalano, A. Nickel: Human health and environmental toxicology. Int. J. Environ. Res. Public Health 2020, 17, 679. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ijomone, O.M.; Okori, S.O.; Ijomone, O.K.; Ebokaiwe, A.P. Sub-acute nickel exposure impairs behavior, alters neuronal microarchitecture, and induces oxidative stress in rats’ brain. Drug Chem. Toxicol. 2018, 41, 377–384. [Google Scholar] [CrossRef] [PubMed]
- Ijomone, O.M.; Olatunji, S.Y.; Owolabi, J.O.; Naicker, T.; Aschner, M. Nickel-induced neurodegeneration in the hippocampus, striatum and cortex; an ultrastructural insight, and the role of caspase-3 and α-synuclein. J. Trace Elem. Med. Biol. 2018, 50, 16–23. [Google Scholar] [CrossRef]
- Weekley, C.M.; Harris, H.H. Which form is that? The importance of selenium speciation and metabolism in the prevention and treatment of disease. Chem. Soc. Rev. 2013, 42, 8870–8894. [Google Scholar] [CrossRef]
- Vinceti, M.; Grill, P.; Malagoli, C.; Filippini, T.; Storani, S.; Malavolti, M.; Michalke, B. Selenium speciation in human serum and its implications for epidemiologic research: A cross-sectional study. J. Trace Elem. Med. Biol. 2015, 31, 1–10. [Google Scholar] [CrossRef]
- Marschall, T.A.; Bornhorst, J.; Kuehnelt, D.; Schwerdtle, T. Differing cytotoxicity and bioavailability of selenite, methylselenocysteine, selenomethionine, selenosugar 1 and trimethylselenonium ion and their underlying metabolic transformations in human cells. Mol. Nutr. Food Res. 2016, 60, 2622–2632. [Google Scholar] [CrossRef]
- Labunskyy, V.M.; Hatfield, D.L.; Gladyshev, V.N. Selenoproteins: Molecular pathways and physiological roles. Physiol. Rev. 2014, 94, 739–777. [Google Scholar] [CrossRef] [Green Version]
- Vinceti, M.; Filippini, T.; Wise, L.A. Environmental selenium and human health: An update. Curr. Environ. Health Rep. 2018, 5, 464–485. [Google Scholar] [CrossRef]
- Rayman, M.P. Selenium intake, status, and health: A complex relationship. Hormones 2020, 19, 9–14. [Google Scholar] [CrossRef] [Green Version]
- Varikasuvu, S.R.; Prasad, S.; Kothapalli, J.; Manne, M. Brain selenium in Alzheimer’s disease (BRAIN SEAD study): A systematic review and meta-analysis. Biol. Trace Elem. Res. 2019, 189, 361–369. [Google Scholar] [CrossRef] [PubMed]
- Cardoso, B.R.; Roberts, B.R.; Bush, A.I.; Hare, D.J. Selenium, selenoproteins and neurodegenerative diseases. Metallomics 2015, 7, 1213–1228. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Robberecht, H.; De Bruyne, T.; Davioud-Charvet, E.; Mackrill, J.; Hermans, N. Selenium status in elderly people: Longevity and age-related diseases. Curr. Pharm. Des. 2019, 25, 1694–1706. [Google Scholar] [CrossRef] [PubMed]
- Berr, C.; Balansard, B.; Arnaud, J.; Roussel, A.M.; Alpérovitch, A.; EVA Study Group. Cognitive decline is associated with systemic oxidative stress: The EVA study. J. Am. Geriat. Soc. 2000, 48, 1285–1291. [Google Scholar] [CrossRef] [PubMed]
- Garcia, T.; Esparza, J.L.; Nogués, M.R.; Romeu, M.; Domingo, J.L.; Gómez, M. Oxidative stress status and RNA expression in hippocampus of an animal model of Alzheimer’s disease after chronic exposure to aluminum. Hippocampus 2010, 20, 218–225. [Google Scholar] [CrossRef]
- McGeer, P.L.; Rogers, J.; McGeer, E.G. Inflammation, antiinflammatory agents, and Alzheimer’s disease: The last 22 years. J. Alzheimers Dis. 2016, 54, 853–857. [Google Scholar] [CrossRef]
- Lin, T.; Liu, G.A.; Perez, E.; Rainer, R.D.; Febo, M.; Cruz-Almeida, Y.; Ebner, N.C. Systemic inflammation mediates age-related cognitive deficits. Front Aging Neurosci. 2018, 10, 236. [Google Scholar] [CrossRef] [Green Version]
- Savaskan, N.E.; Bräuer, A.U.; Kühbacher, M.; Eyüpoglu, I.Y.; Kyriakopoulos, A.; Ninnemann, O.; Behne, D.; Nitsch, R. Selenium deficiency increases susceptibility to glutamate-induced excitotoxicity. FASEB J. 2003, 17, 112–114. [Google Scholar] [CrossRef]
- Prabhu, K.S.; Zamamiri-Davis, F.; Stewart, J.B.; Thompson, J.T.; Sordillo, L.M.; Reddy, C.C. Selenium deficiency increases the expression of inducible nitric oxide synthase in RAW 264.7 macrophages: Role of nuclear factor-κB in up-regulation. Biochem. J. 2002, 366, 203–209. [Google Scholar] [CrossRef] [Green Version]
- Schweizer, U.; Schomburg, L. Selenium, selenoproteins and brain function. In Selenium; Hatfield, D.L., Berry, M.J., Gladyshev, V.N., Eds.; Springer: Boston, MA, USA, 2006; pp. 233–248. ISBN 978-0-387-33827-9. [Google Scholar]
- Pitts, M.W.; Kremer, P.M.; Hashimoto, A.C.; Torres, D.J.; Byrns, C.N.; Williams, C.S.; Berry, M.J. Competition between the brain and testes under selenium-compromised conditions: Insight into sex differences in selenium metabolism and risk of neurodevelopmental disease. J. Neurosci. 2015, 35, 15326–15338. [Google Scholar] [CrossRef] [Green Version]
- Berr, C. Cognitive impairment and oxidative stress in the elderly: Results of epidemiological studies. Biofactors 2000, 13, 205–209. [Google Scholar] [CrossRef] [PubMed]
- Berr, C.; Arnaud, J.; Akbaraly, T.N. Selenium and cognitive impairment: A brief-review based on results from the EVA study. Biofactors 2012, 38, 139–144. [Google Scholar] [CrossRef] [PubMed]
- Cardoso, B.R.; Ong, T.P.; Jacob-Filho, W.; Jaluul, O.; Freitas, M.I.Á.; Cozzolino, S.M.F. Nutritional status of selenium in Alzheimer’s disease patients. Br. J. Nutr. 2010, 103, 803–806. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, S.; Jin, Y.; Hall, K.S.; Liang, C.; Unverzagt, F.W.; Ji, R.; Murrell, J.R.; Cao, J.; Shen, J.; Ma, F.; et al. Selenium level and cognitive function in rural elderly Chinese. Am. J. Epidemiol. 2007, 165, 955–965. [Google Scholar] [CrossRef] [Green Version]
- Reddy, V.S.; Bukke, S.; Dutt, N.; Rana, P.; Pandey, A.K. A systematic review and meta-analysis of the circulatory, erythrocellular and CSF selenium levels in Alzheimer’s disease: A metal meta-analysis (AMMA study-I). J. Trace Elem. Med. Biol. 2017, 42, 68–75. [Google Scholar] [CrossRef]
- Gao, S.; Jin, Y.; Hall, K.S.; Liang, C.; Unverzagt, F.W.; Ma, F.; Cheng, Y.; Shen, J.; Cao, J.; Matesan, J.; et al. Selenium level is associated with apoE ε4 in rural elderly Chinese. Public Health Nutr. 2009, 12, 2371–2376. [Google Scholar] [CrossRef] [Green Version]
- Vinceti, M.; Chiari, A.; Eichmüller, M.; Rothman, K.J.; Filippini, T.; Malagoli, C.; Weuve, J.; Tondelli, M.; Zamboni, G.; Nichelli, F.; et al. A selenium species in cerebrospinal fluid predicts conversion to Alzheimer’s dementia in persons with mild cognitive impairment. Alzheimers Res. Ther. 2017, 9, 100. [Google Scholar] [CrossRef] [Green Version]
- McClain, C.J.; McClain, M.; Barve, S.; Boosalis, M.G. Trace metals and the elderly. Clin. Geriatr. Med. 2002, 18, 801–818. [Google Scholar] [CrossRef]
- Cardoso, B.R.; Bandeira, V.S.; Jacob-Filho, W.; Cozzolino, S.M.F. Selenium status in elderly: Relation to cognitive decline. J. Trace Elem. Med. Biol. 2014, 28, 422–426. [Google Scholar] [CrossRef]
- Forte, G.; Deiana, M.; Pasella, S.; Baralla, A.; Occhineri, P.; Mura, I.; Madeddu, R.; Muresu, E.; Sotgia, S.; Zinellu, A.; et al. Metals in plasma of nonagenarians and centenarians living in a key area of longevity. Exp. Gerontol. 2014, 60, 197–206. [Google Scholar] [CrossRef]
- Alis, R.; Santos-Lozano, A.; Sanchis-Gomar, F.; Pareja-Galeano, H.; Fiuza-Luces, C.; Garatachea, N.; Lucia, A.; Emanuele, E. Trace elements levels in centenarian ‘dodgers’. J. Trace Elem. Med. Biol. 2016, 35, 103–106. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.W.; Shi, X.M.; Yin, Z.X.; Liu, Y.Z.; Zhai, Y.; Zeng, Y. Investigation and analysis of plasma trace elements of oldest elderly in longevity areas in China. Zhonghua Yu Fang Yi Xue Za Zhi 2010, 44, 119–122. [Google Scholar] [PubMed]
- Cai, Z.; Zhang, J.; Li, H. Selenium, aging and aging-related diseases. Aging Clin. Exp. Res. 2018, 1–13. [Google Scholar] [CrossRef] [PubMed]
- INE. Tábuas de Mortalidade em Portugal [Mortality Tables in Portugal]. Available online: https://www.ine.pt/xportal/xmain?xpid=INE&xpgid=ine_destaques&DESTAQUESdest_boui=354096866&DESTAQUESmodo=2&xlang=pt (accessed on 2 April 2020).
RES n = 20 | CTR n = 20 | |
---|---|---|
Marital Status, n (%) | ||
Single | 2 (10) | 1 (5) |
Married | 2 (10) | 12 (60) |
Divorced | 3 (15) | 1 (5) |
Widowed | 13 (65) | 6 (30) |
Occupation/professional activity, n (%) | ||
Agriculture/fishery | 6 (30) | 1 (5) |
Industry/construction | 4 (20) | 3 (15) |
Commerce/Services | 8 (40) | 14 (70) |
Housewife | 2 (10) | 3 (10) |
Medical History, n (%) | ||
Diabetes | 4 (20) | 2 (10) |
Dyslipidemia | 12 (60) | 9 (45) |
Cardiovascular diseases | 16 (80) | 15 (75) |
RES Group (µg/g) | Literature Data | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Non-Exposed Individuals [74] | Healthy Centenarians [75] | |||||||||||
Min-Max | M | SD | Md | Min-Max | M | SD | Md | Min-Max | M | SD | Md | |
Al | 3.57–54.61 | 18.93 | 14.22 | 14.42 | 12.00–137.00 | 36.00 | 22.00 | 32.00 | - | - | - | - |
As | 0.07–0.30 | 0.12 | 0.06 | 0.11 | 0.07–1.09 | 0.27 | 0.19 | 0.22 | - | - | - | - |
Ba | 0.11–2.21 | 0.64 | 0.73 | 0.31 | 0.28–3.99 | 1.34 | 1.35 | 0.89 | 0.94–22.92 | 5.10 | 3.92 | 3.85 |
Cd | 0.002–0.06 | 0.01 | 0.01 | 0.01 | 0.01–0.44 | 0.11 | 0.18 | 0.06 | 0.004–0.19 | 0.03 | 0.03 | 0.02 |
Co | 0.003–0.04 | 0.01 | 0.01 | 0.01 | 0.01–0.12 | 0.03 | 0.03 | 0.02 | 0.01–0.64 | 0.10 | 0.10 | 0.07 |
Cr | 0.25–0.93 | 0.61 | 0.20 | 0.60 | 0.22–3.20 | 1.16 | 1.05 | 0.76 | 0.08–2.51 | 0.82 | 0.44 | 0.82 |
Cu | 2.66–7.40 | 4.67 | 1.32 | 4.83 | 4.20–17.00 | 8.40 | 3.50 | 7.60 | 2.02–8.53 | 3.71 | 0.99 | 3.55 |
Fe | 7.31–49.84 | 24.01 | 13.25 | 20.06 | 12.00–189.00 | 42.00 | 30.00 | 37.00 | 16.52–692.00 | 154.40 | 124.80 | 116.70 |
Hg | 0.12–0.85 | 0.42 | 0.20 | 0.42 | 0.03–0.31 | 0.12 | 0.098 | 0.098 | - | - | - | - |
Li | 0.005–0.18 | 0.04 | 0.04 | 0.02 | 0.01–0.25 | 0.07 | 0.07 | 0.05 | 0.02–2.07 | 0.31 | 0.32 | 0.23 |
Mn | 0.04–2.93 | 0.58 | 0.79 | 0.17 | 0.19–3.30 | 0.90 | 0.75 | 0.65 | 0.21–15.40 | 3.09 | 2.18 | 2.62 |
Ni | 0.09–2.98 | 0.93 | 1.04 | 0.36 | 0.14–6.95 | 1.65 | 2.20 | 0.84 | 0.02–3.67 | 0.95 | 0.85 | 0.66 |
Pb | 0.07–1.73 | 0.38 | 0.38 | 0.30 | 0.27–4.75 | 1.38 | 1.14 | 1.06 | 0.13–9.61 | 1.86 | 1.81 | 1.33 |
Sb | 0.008–0.13 | 0.04 | 0.04 | 0.03 | 0.01–0.13 | 0.05 | 0.05 | 0.04 | - | - | - | - |
Se | 0.60–1.03 | 0.803 | 0.13 | 0.80 | 0.62–1.53 | 0.94 | 0.21 | 0.93 | 0.24–0.70 | 0.44 | 0.11 | 0.44 |
Sn | 0.01–1.20 | 0.33 | 0.36 | 0.17 | 0.11–2.56 | 0.63 | 0.51 | 0.48 | - | - | - | - |
Sr | 0.07–2.24 | 0.48 | 0.53 | 0.27 | 0.17–1.39 | 0.43 | 0.21 | 0.39 | 1.40–18.50 | 6.20 | 2.47 | 5.80 |
Ti | 3.68–6.75 | 5.14 | 0.77 | 5.15 | 0.94–16.10 | 4.46 | 5.01 | 2.71 | - | - | - | - |
V | 0.05–0.38 | 0.120 | 0.07 | 0.10 | 0.02–0.48 | 0.08 | 0.05 | 2.71 | - | - | - | - |
Zn | 88.65–219.31 | 144.10 | 39.15 | 137.34 | 80.00–191.00 | 120.00 | 29.00 | 116.00 | 93.00–326.00 | 148.00 | 36.00 | 138.00 |
Linear Regression Models | R2adjusted | Model Significance | |
---|---|---|---|
MMSE-1 | MMSE = 14.258 + 3.259 Ni | 0.197 | p = 0.029 |
MMSE-2 | MMSE = 10.329 + 1.436 Education + 3.700 Ni | 0.288 | p = 0.022 |
MoCA-1 | MoCA = 7.503 + 3.369 Ni | 0.331 | p = 0.029 |
MoCA-2 | MoCA = −9.258 + 26.821 Se | 0.361 | p = 0.023 |
MoCA-3 | MoCA = −9.460 + 2.851 Ni + 23.017 Se | 0.622 | p = 0.005 |
MoCA-4 | MoCA = −16.147 + 1.556 Education + 3.525 Ni + 24.022 Se | 0.679 | p = 0.007 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gerardo, B.; Cabral Pinto, M.; Nogueira, J.; Pinto, P.; Almeida, A.; Pinto, E.; Marinho-Reis, P.; Diniz, L.; Moreira, P.I.; Simões, M.R.; et al. Associations between Trace Elements and Cognitive Decline: An Exploratory 5-Year Follow-Up Study of an Elderly Cohort. Int. J. Environ. Res. Public Health 2020, 17, 6051. https://doi.org/10.3390/ijerph17176051
Gerardo B, Cabral Pinto M, Nogueira J, Pinto P, Almeida A, Pinto E, Marinho-Reis P, Diniz L, Moreira PI, Simões MR, et al. Associations between Trace Elements and Cognitive Decline: An Exploratory 5-Year Follow-Up Study of an Elderly Cohort. International Journal of Environmental Research and Public Health. 2020; 17(17):6051. https://doi.org/10.3390/ijerph17176051
Chicago/Turabian StyleGerardo, Bianca, Marina Cabral Pinto, Joana Nogueira, Paula Pinto, Agostinho Almeida, Edgar Pinto, Paula Marinho-Reis, Luísa Diniz, Paula I. Moreira, Mário R. Simões, and et al. 2020. "Associations between Trace Elements and Cognitive Decline: An Exploratory 5-Year Follow-Up Study of an Elderly Cohort" International Journal of Environmental Research and Public Health 17, no. 17: 6051. https://doi.org/10.3390/ijerph17176051