Mineral elements and adiposity-related consequences in adolescents with intellectual disabilities.
Adipokines
Adolescence
Intellectual disability
Mineral elements
Oxidative stress
Journal
BMC molecular and cell biology
ISSN: 2661-8850
Titre abrégé: BMC Mol Cell Biol
Pays: England
ID NLM: 101741148
Informations de publication
Date de publication:
20 Sep 2023
20 Sep 2023
Historique:
received:
14
06
2023
accepted:
12
09
2023
medline:
22
9
2023
pubmed:
21
9
2023
entrez:
20
9
2023
Statut:
epublish
Résumé
Patients with intellectual disabilities are shown to have a limited capacity for cooperation, communication,and other biological consequences, which significantly require a specialized interest in healthcare professionals worldwide. In this respect, the present study was designed to evaluate the levels mineral elements, and their correlation with oxidative stress markers and adiposity markers; leptin (L), adiponectin (A), and L/A ratio in adolescents with intellectual disabilities. A total of 350 schoolchildren aged (12-18 years) were randomly invited to participate in this prospective, observational study. Only 300 participants agreed to participate in this study. According to Intelligence quotients scores (IQ) measured by WISC-III, the participants were classified into two groups; the healthy control group (no = 180; IQ = 90-114); and the moderate intellectual disability (MID) group (no = 120; IQ = 35-49). Adiposity markers; body mass index (BMI), waist-to-hip ratio (WHR), waist-to-height ratio (WHtR), physical activity scores, adipokines biomarkers; leptin, adiponectin, L/A ratio, oxidative stress, and plasma mineral elements were evaluated by prevalidated questionnaires, inductively coupled plasma-mass spectrometry (ICP-MS), colorimetric, and immunoassay techniques. Intellectual disability of moderate type was reported in 40% of the studied populations most of them are men aged 12-18 years (66.6% for men vs. 33.3 for females). Obesity was shown to be associated with the degree of intellectual disability of the students. There was a significant (P = 0.001) increase in the BMI, WHR, and WHtR scores as obesity markers with poor physical activity (P = 0.01) in students with poor disability compared to healthy controls (HC). The levels of leptin (P = 0.001), adiponectin (P = 0.01), and L/A ratio (P = 0.01) as adiposity biomarkers were significantly increased in students with MID compared to healthy controls. Also, oxidative stress measured by malondialdehyde (MDA) (P = 0.01) and total antioxidant capacity (TAC) (P = 0.01) were significantly increased in students with MID compared to healthy control subjects. In addition, mineral elements were shown to be linked with intellectual disability. The data showed that the levels of Fe, Mn, Zn, Hg, Pb, Ca, Cr, Mg, and Ni significantly (P = 0.001) increased, and the levels of Al, Na, K, Cu, and Zn/Cu ratio significantly (P = 0.001) decreased in subjects with MID compared to healthy controls. Correlation analysis concluded that changes in mineral elements significantly correlated with adiposity markers, oxidative stress, and the scores of intellectual disability (WISC III-IQ score). The intellectual disability of moderate type (MID) was associated with abnormal changes in the levels of essential mineral elements and adipokines and increased levels of cellular oxidative stress. Thus, evaluating plasma mineral elements and adipokines levels could be a potential diagnostic parameter for diagnosing MID.
Sections du résumé
BACKGROUND
BACKGROUND
Patients with intellectual disabilities are shown to have a limited capacity for cooperation, communication,and other biological consequences, which significantly require a specialized interest in healthcare professionals worldwide.
AIM
OBJECTIVE
In this respect, the present study was designed to evaluate the levels mineral elements, and their correlation with oxidative stress markers and adiposity markers; leptin (L), adiponectin (A), and L/A ratio in adolescents with intellectual disabilities.
METHODS
METHODS
A total of 350 schoolchildren aged (12-18 years) were randomly invited to participate in this prospective, observational study. Only 300 participants agreed to participate in this study. According to Intelligence quotients scores (IQ) measured by WISC-III, the participants were classified into two groups; the healthy control group (no = 180; IQ = 90-114); and the moderate intellectual disability (MID) group (no = 120; IQ = 35-49). Adiposity markers; body mass index (BMI), waist-to-hip ratio (WHR), waist-to-height ratio (WHtR), physical activity scores, adipokines biomarkers; leptin, adiponectin, L/A ratio, oxidative stress, and plasma mineral elements were evaluated by prevalidated questionnaires, inductively coupled plasma-mass spectrometry (ICP-MS), colorimetric, and immunoassay techniques.
RESULTS
RESULTS
Intellectual disability of moderate type was reported in 40% of the studied populations most of them are men aged 12-18 years (66.6% for men vs. 33.3 for females). Obesity was shown to be associated with the degree of intellectual disability of the students. There was a significant (P = 0.001) increase in the BMI, WHR, and WHtR scores as obesity markers with poor physical activity (P = 0.01) in students with poor disability compared to healthy controls (HC). The levels of leptin (P = 0.001), adiponectin (P = 0.01), and L/A ratio (P = 0.01) as adiposity biomarkers were significantly increased in students with MID compared to healthy controls. Also, oxidative stress measured by malondialdehyde (MDA) (P = 0.01) and total antioxidant capacity (TAC) (P = 0.01) were significantly increased in students with MID compared to healthy control subjects. In addition, mineral elements were shown to be linked with intellectual disability. The data showed that the levels of Fe, Mn, Zn, Hg, Pb, Ca, Cr, Mg, and Ni significantly (P = 0.001) increased, and the levels of Al, Na, K, Cu, and Zn/Cu ratio significantly (P = 0.001) decreased in subjects with MID compared to healthy controls. Correlation analysis concluded that changes in mineral elements significantly correlated with adiposity markers, oxidative stress, and the scores of intellectual disability (WISC III-IQ score).
CONCLUSION
CONCLUSIONS
The intellectual disability of moderate type (MID) was associated with abnormal changes in the levels of essential mineral elements and adipokines and increased levels of cellular oxidative stress. Thus, evaluating plasma mineral elements and adipokines levels could be a potential diagnostic parameter for diagnosing MID.
Identifiants
pubmed: 37730529
doi: 10.1186/s12860-023-00490-5
pii: 10.1186/s12860-023-00490-5
pmc: PMC10512604
doi:
Substances chimiques
Leptin
0
Adiponectin
0
Minerals
0
Adipokines
0
Types de publication
Observational Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
29Subventions
Organisme : Researchers Supporting Project number (RSP2023R382), King Saud University, Riyadh, Saudi Arabia.
ID : RSP2023R382
Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Al-Saleh E, Nandakumaran M, Al-Harmi J, Sadan T, Al-Enezi H. Maternal-fetal status of copper, iron, molybdenum, selenium, and zinc in obese pregnant women in late gestation. Biol Trace Elem Res. 2006;113:113–23.
pubmed: 17194914
Zatterale F, Longo M, Naderi J, Raciti GA, Desiderio A, Miele C, et al. Chronic adipose tissue inflammation linking obesity to insulin resistance and type 2 diabetes. Front Physiol. 2020;29(10):1607.
Kumar R, Mal K, Razaq MK, Magsi M, Memon MK, Memon S, Afroz MN, Siddiqui HF, Rizwan A. Association of leptin with obesity and insulin resistance. Cureus. 2020;12(12): e12178.
pubmed: 33489589
pmcid: 7815269
Kojta I, Chacińska M, Błachnio-Zabielska A. Obesity, bioactive lipids, and adipose tissue inflammation in insulin resistance. Nutrients. 2020;12(5):1305.
pubmed: 32375231
pmcid: 7284998
Robinson E, Boyland E, Chisholm A, Harrold J, Maloney NG, Marty L, et al. Obesity, eating behavior and physical activity during COVID-19 lockdown: a study of UK adults. Appetite. 2021;156: 104853.
pubmed: 33038479
Lobstein T, Baur L, Uauy R. IASO international obesity TaskForce: obesity in children and young people: a crisis in public health. Obes Rev. 2004;5(1):4–104.
pubmed: 15096099
Krebs NF, Jacobson MS. American academy of pediatrics committee on nutrition: prevention of pediatric overweight and obesity. Pediatrics. 2003;112(2):424–30.
pubmed: 12897303
Jurado-Castro JM, Gil-Campos M, Gonzalez-Gonzalez H, Llorente-Cantarero FJ. Evaluation of physical activity and lifestyle interventions focused on school children with obesity using accelerometry: a systematic review and meta-analysis. Int J Environ Res Public Health. 2020;17(17):6031.
pubmed: 32825085
pmcid: 7503305
Thaler JP, Schwartz MW. Minireview: inflammation and obesity pathogenesis: the hypothalamus heats up. Endocrinology. 2010;151:4109–15.
pubmed: 20573720
pmcid: 2940486
Pengelly CD, Morris J. Body mass index and weightdistribution. Scott Med J. 2009;54(3):17–21.
pubmed: 19725277
Hu K, Staiano AE. Trends in obesity prevalence among children and adolescents aged 2 to 19 years in the US from 2011 to 2020. JAMA Pediatr. 2022;176(10):1037–9.
pubmed: 35877133
pmcid: 9315946
Ben-Sefer E, Ben-Natan M, Ehrenfeld M. Childhood obesity: current literature, policy and implications for practice. Int Nurs Rev. 2009;56(2):166–73.
pubmed: 19646165
García OP, Long KZ, Rosado JL. Impact of micronutrient deficiencies on obesity. Nutr Rev. 2009;67(10):559–72.
pubmed: 19785688
García OP, Ronquillo D, Caamaño MD, Camacho M, Long KZ, Rosado JL. Zinc, vitamin A, and vitamin C status are associated with leptin concentrations and obesity in Mexican women: results from a cross-sectional study. Nutr Metab. 2012;9:1–9.
Zavala G, Long KZ, García OP, del Carmen CM, Aguilar T, Salgado LM, et al. Specific micronutrient concentrations are associated with inflammatory cytokines in a rural population of Mexican women with a high prevalence of obesity. Br J Nutr. 2013;109(4):686–94.
pubmed: 22640991
Aeberli I, Hurrell RF, Zimmermann MB. Overweight children have higher circulating hepcidin concentrations and lower iron status but have dietary iron intakes and bioavailability comparable with normal weight children. Int J Obes (Lond). 2009;33:1111–7.
pubmed: 19636315
da Silva LD, da Veiga GV, Ramalho RA. Association of serum concentrations of retinol and carotenoids with overweight in children and adolescents. Nutrition. 2007;23:392–7.
Huang J, Weinstein SJ, Moore SC, Derkach A, Hua X, Liao LM, et al. Serum metabolomic profiling of all-cause mortality: a prospective analysis in the alpha-tocopherol, beta-carotene cancer prevention (ATBC) study cohort. Am J Epidemiol. 2018;187(8):1721–32.
pubmed: 29390044
pmcid: 6070082
Molnar D, Decsi T, Koletzko B. Reduced antioxidant status in obese children with multimetabolic syndrome. Int J Obes Relat Metab Disord. 2004;28:1197–202.
pubmed: 15314634
Garcia-Diaz DF, Campion J, Milagro FI, Boque N, Moreno-Aliaga MJ, Martinez JA. Vitamin C inhibits leptin secretion and some glucose/lipid metabolic pathways in primary rat adipocytes. J Mol Endocrinol. 2010;45:33–43.
pubmed: 20400526
Kelishadi R, Hashemipour M, Adeli K, Tavakoli N, Movahedian-Attar A, Shapouri J, et al. Effect of zinc supplementation on markers of insulin resistance, oxidative stress, and inflammation among prepubescent children with metabolic syndrome. Metab Syndr Relat Disord. 2010;8:505–10.
pubmed: 21028969
Shen XH, Tang QY, Huang J, Cai W. Vitamin E regulates adipocytokine expression in a rat model of dietary-induced obesity. Exp Biol Med (Maywood). 2010;235:47–51.
pubmed: 20404018
Grondhuis SN, Aman MG. Overweight and obesity in youth with developmental disabilities: a call to action. J Intellect Disabil Res. 2014;58:787–99.
Phillips KL, Schieve LA, Visser S, Boulet S, Sharma AJ, Kogan MD, et al. Prevalence and impact of unhealthy weight in a national sample of US adolescents with autism and other learning and behavioral disabilities. Matern Child Health J. 2014;18:1964–75.
pubmed: 24553796
pmcid: 5328414
Slevin E, Truesdale-Kennedy M, McConkey R, Livingstone B, Fleming P. Obesity and overweight in intellectual and non-intellectually disabled children. J Intellect Disabil Res. 2014;58:211–20.
pubmed: 22957929
Bennett EA, Kolko RP, Chia L, Elliott JP, Kalarchian MA. Treatment of obesity among youth with intellectual and developmental disabilities: an emerging role for telenursing. West J Nurs Res. 2017;39(8):1008–27. https://doi.org/10.1177/0193945917697664 .
doi: 10.1177/0193945917697664
pmcid: 5913737
Segal M, Eliasziw M, Phillips S, Bandini L, Curtin C, Kral T, et al. Intellectual disability is associated with increased risk for obesity in a nationally representative sample of U.S. children. Disabil Health J. 2016;9:392–8.
pubmed: 26785808
Stanish HI, Curtin C, Must A, Phillips S, Maslin M, Bandini LG. Physical activity enjoyment, perceived barriers, and beliefs among adolescents with and without intellectual disabilities. J Phys Act Health. 2016;13:102–10.
pubmed: 25830443
Alghadir AH, Iqbal ZA, Gabr SA. Differences among Saudi and expatriate students: body composition indices, sitting time associated with media use and physical activity pattern. Int J Environ Res Public Health. 2020;17(3):E832. https://doi.org/10.3390/ijerph17030832 .
doi: 10.3390/ijerph17030832
Curtin C, Bandini LG, Must A, Gleason J, Lividini K, Phillips S, et al. Parent support improves weight loss in adolescents and young adults with down syndrome. J Pediatr. 2013;163:1402–8.
pubmed: 23968742
Rodríguez-Barranco M, Lacasaña M, Aguilar-Garduño C, Alguacil J, Gil F, González-Alzaga B, et al. Association of arsenic, cadmium and manganeseexposure with neurodevelopment and behavioural disorders in children: a systematic review andmeta-analysis. Sci Total Environ. 2013;454:562–77.
pubmed: 23570911
Grandjean P, Weihe P, Debes F, Choi AL, Budtz-Jørgensen E. Neurotoxicity from prenatal and postnatal exposure to methylmercury. Neurotoxicol Teratol. 2014;43:39–44.
pubmed: 24681285
pmcid: 4066386
Khan K, Wasserman GA, Liu X, Ahmed E, Parvez F, Slavkovich V, et al. Manganese exposure from drinking water and children’s academic achievement. Neurotoxicology. 2012;33:91–7.
pubmed: 22182530
Selevan SG, Rice DC, Hogan KA, Euling SY, Pfahles-Hutchens A, Bethel J. Blood lead concentration and delayed puberty in girls. N Engl J Med. 2003;348:1527–36.
pubmed: 12700372
Kim Y, Cho S-C, Kim B-N, Hong Y-C, Shin M-S, Yoo H-J, et al. Association between blood lead levels(<5μg/dL)and inattention-hyperactivity and neurocognitive profiles in school-aged Korean children. Sci Total Environ. 2010;408:5737–43.
pubmed: 20825975
Bellinger DC. Prenatal exposures to environmental chemicals and children’s neurodevelopment: An update. Saf Health Work. 2013;4:1–11.
pubmed: 23515885
pmcid: 3601292
Vigeh M, Yokoyama K, Matsukawa T, Shinohara A, Ohtani K. Low level prenatal blood lead adversely affects early childhood mental development. J Child Neurol. 2014;29(10):1305–11. https://doi.org/10.1177/0883073813516999 .
doi: 10.1177/0883073813516999
pubmed: 24532811
Koivula MJ, Kanerva M, Salminen J-P, Nikinmaa M, Eeva T. Metal pollution indirectly increases oxidative stress in great tit (Parus major) nestlings. Environ Res. 2011;111:362–70.
pubmed: 21295293
Grotto D, Santa Maria L, Boeira S, Valentini J, Charão M, Moro A, et al. Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography-visible detection. J Pharm Biomed Anal. 2007;43:619–24.
pubmed: 16949242
Canivez G, Watkins M. Exploratory and higher-order factor analyses of the Wechsler Adult Intelligence Scale-Fourth Edition (WAIS-IV) adolescent subsample. Sch Psychol Q. 2010;25(4):223–35.
Wechsler D. Wechsler adult intelligence scale–Fourth Edition (WAIS–IV). Vol. 22(498). San Antonio: NCS Pearson; 2008. p. 1.
Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. Br Med J. 2000;320:1–6.
Fan Y, Wang R, Ding L, Meng Z, Zhang Q, Shen Y, et al. Waist circumference and its changes are more strongly associated with the risk of type 2 diabetes than body mass index and changes in body weight in Chinese adults. J Nutr. 2020;150(5):1259–65.
pubmed: 32006008
Al-Rawaf HA. Circulating microRNAs and adipokines as markers of metabolic syndrome in adolescents with obesity. Clin Nutr. 2019;38(5):2231–8. https://doi.org/10.1016/j.clnu.2018.09.024 .
doi: 10.1016/j.clnu.2018.09.024
pubmed: 30309709
Cabral Pinto MM, Marinho-Reis P, Almeida A, Pinto E, Neves O, Inácio M, 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(22):4560. https://doi.org/10.3390/ijerph16224560 .
doi: 10.3390/ijerph16224560
pubmed: 31752166
pmcid: 6888438
Carmeli E, Imam B, Bachar A, Merrick J. Inflammation and oxidative stress as biomarkers of premature aging in persons with intellectual disability. Res Dev Disabil. 2012;33(2):369–75.
pubmed: 22119683
Alghadir AH, Gabr SA, Al-Eisa ES. Effects of moderate aerobic exercise on cognitive abilities and redox state biomarkers in older adults. Oxid Med Cell Longev. 2016;2016:2545168. https://doi.org/10.1155/2016/2545168 .
doi: 10.1155/2016/2545168
pubmed: 27195073
pmcid: 4852338
Alghadir AH, Gabr SA, Anwer S, Al-Eisa E. Fatigue and oxidative stress response to physical activity in type 2 diabetic patients. Int J Diabetes Dev Ctries. 2016;36:59–64.
Rusdiana A. Analysis differences of Vo2max between direct and indirect measurement in badminton, cycling and rowing. Int J Appl Exerc Physiol. 2020;9(3):162–70.
Zhou N, Wong HM, Wen YF, Mcgrath C. Oral health status of children and adolescents with intellectual disabilities: a systematic review and meta-analysis. Dev Med Child Neurol. 2017;59:019–1026.
Oliveira JS, Prado Júnior RR, de Sousa Lima KR, de Oliveira AH, Moita Neto JM, Mendes RF. Intellectual disability and impact on oral health: a paired study. Spec Care Dentist. 2013;33(6):262–8.
pubmed: 24164223
Collins K, Staples K. The role of physical activity in improving physical fitness in children with intellectual and developmental disabilities. Res Dev Disabil. 2017;69:49–60.
pubmed: 28818714
Martínez-Leal R, Salvador-Carulla L, Gutiérrez-Colosía MR, Nadal M, Novell-Alsina R, Martorell A, et al. Health among persons with intellectual disability in Spain: the European POMONA-II study. Rev Neurol. 2011;53(7):406–14.
pubmed: 21948011
Smyth P, McDowell C, Leslie JC, Leader G, Donnelly M, Simpson E, et al. Managing weight: what do people with an intellectual disability want from mobile technology? Stud Health Technol Inform. 2017;242:273–8.
pubmed: 28873810
Basil JS, Santoro SL, Martin LJ, Healy KW, Chini BA, Saal HM. Retrospective study of obesity in children with Down Syndrome. J Pediatr. 2016;173:143–8.
pubmed: 26987801
Martínez-Zaragoza F, Campillo-Martínez J, Ato-García M. Effects on physical health of a multicomponent programme for overweight and obesity for adults with intellectual disabilities. J Appl Res Intellect Disabil. 2016;29(3):250–65.
pubmed: 25847077
Lobenius-Palmér K, Sjöqvist B, Hurtig-Wennlöf A, Lundqvist LO. Accelerometer-assessed physical activity and sedentary time in youth with disabilities. Adapt Phys Activ Q. 2017;26:1–19.
Mikulovic J, Marcellini A, Compte R, Duchateau G, Vanhelst J, Fardy PS, et al. Prevalence of overweight in adolescents with intellectual deficiency: Differences in socio-educative context, physical activity and dietary habits. Appetite. 2011;56:403–7.
pubmed: 21146573
Weil E, Wachterman M, McCarthy EP, Davis RB, O’Day B, Iezzoni LI, et al. Obesity among adults with disabling conditions. JAMA. 2002;288(10):1265–8.
pubmed: 12215134
Fasshauer M, Bluher M. Adipokines in health and disease. Trends Pharmacol Sci. 2015;36(7):461e70.
Philips EM, Santos S, Trasande L, Aurrekoetxea JJ, Barros H, von Berg A, et al. Changes in parental smoking during pregnancy and risks of adverse birth outcomes and childhood overweight in Europe and North America: An individual participant data meta-analysis of 229,000 singleton births. PLoS Med. 2020;17(8): e1003182.
pubmed: 32810184
pmcid: 7433860
Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW, et al. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med. 2004;350(23):2362e74.
Pérez-Pérez A, Vilariño-García T, Fernández-Riejos P, Martín-González J, Segura-Egea JJ, Sánchez-Margalet V. Role of leptin as a link between metabolism and the immune system. Cytokine Growth Factor Rev. 2017;35:71–84. https://doi.org/10.1016/j.cytogfr.2017.03.001 .
doi: 10.1016/j.cytogfr.2017.03.001
pubmed: 28285098
Behl S, Mehta S, Pandey MK. Abnormal levels of metal micronutrients and autism spectrum disorder: a perspective review. Front Mol Neurosci. 2020;13:586209. https://doi.org/10.3389/fnmol.2020.586209 .
doi: 10.3389/fnmol.2020.586209
pubmed: 33362464
pmcid: 7759187
Skalny AV, Mazaletskaya AL, Ajsuvakova OP, Bjørklund G, Skalnaya MG, Chernova LN, et al. Magnesium status in children with attention-deficit/hyperactivity disorder and/or autism spectrum disorder. Soa Chongsonyon Chongsin Uihak. 2020;31(1):41–5. https://doi.org/10.5765/jkacap.190036 .
doi: 10.5765/jkacap.190036
pubmed: 32612412
pmcid: 7324841
Barišić A, Ravančić ME, Majstorivić D, Vraneković J. Micronutrient status in children and adolescents with Down syndrome: systematic review and meta-analysis. J Intellect Disabil Res. 2023;67(8):701–19. https://doi.org/10.1111/jir.13042 .
doi: 10.1111/jir.13042
pubmed: 37218392
Grabeklis AR, Skalny AV, Skalnaya AA, Zhegalova IV, Notova SV, Mazaletskaya AL, et al. Hair mineral and trace element content in children with down’s syndrome. Biol Trace Elem Res. 2019;188:230–8.
pubmed: 30209729
Fiore M, Barone R, Copat C, Grasso A, Cristaldi A, Rizzo R, et al. Metal and essential element levels in hair and association with autism severity. J Trace Elem Med Biol. 2020;57: 126409.
pubmed: 31630927
Beard JL. Iron biology in immune function, muscle metabolism and neuronal functioning. J Nutr. 2001;131(2S-2):568S-579S. https://doi.org/10.1093/jn/131.2.568S . discussion 580S.
doi: 10.1093/jn/131.2.568S
pubmed: 11160590
Murray-Kolb LE, Beard JL. Iron treatment normalizes cognitive functioning in young women. Am J Clin Nutr. 2007;85(3):778–87. https://doi.org/10.1093/ajcn/85.3.778 .
doi: 10.1093/ajcn/85.3.778
pubmed: 17344500
Hambidge KM, Krebs NF. Zinc deficiency: a special challenge. J Nutr. 2007;137(4):1101–5. https://doi.org/10.1093/jn/137.4.1101 .
doi: 10.1093/jn/137.4.1101
pubmed: 17374687
Osredkar J, Sustar N. Copper and zinc, biological role and significance of copper/zinc imbalance. J Clinic Toxicol S. 2011;3(2161):0495.
Rao TS, Asha MR, Ramesh BN, Rao KJ. Understanding nutrition, depression and mental illnesses. Indian J Psychiatry. 2008;50(2):77.
pubmed: 19742217
pmcid: 2738337
Li Z, Liu Y, Wei R, Yong VW, Xue M. The important role of zinc in neurological diseases. Biomolecules. 2022;13(1):28.
pubmed: 36671413
pmcid: 9855948
Indika NL, Frye RE, Rossignol DA, Owens SC, Senarathne UD, Grabrucker AM, et al. The rationale for vitamin, mineral, and cofactor treatment in the precision medical care of autism spectrum disorder. J Personal Med. 2023;13(2):252.
Shazia Q, Mohammad ZH, Rahman T, Shekhar HU. Correlation of oxidative stress with serum trace element levels and antioxidant enzyme status in Beta thalassemia major patients: a review of the literature. Anemia. 2012;2012: 270923.
pubmed: 22645668
pmcid: 3357501
Zoroddu MA, Aaseth J, Crisponi G, Medici S, Peana M, Nurchi VM. The essential metals for humans: a brief overview. J Inorg Biochem. 2019;195:120–9.
pubmed: 30939379
Bhattacharya PT, Misra SR, Hussain M. Nutritional aspects of essential trace elements in oral health and disease: an extensive review. Scientifica (Cairo). 2016;2016:1–12. https://doi.org/10.1155/2016/5464373 .
Alghadir AH, Gabr SA, Al-Eisa E. Effects of physical activity on trace elements and depression related biomarkers in children and adolescents. Biol Trace Elem Res. 2016;172(2):299–306. https://doi.org/10.1007/s12011-015-0601-3 .
Watanabe K, Tanaka T, Shigemi T, Hayashida Y, Maki K. Mn and Cu concentrations in mixed saliva of elementary school children in relation to sex, age, and dental caries. J Trace Elem Med Biol. 2009;23:93–9.
pubmed: 19398056