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Supplementation of the maternal diet with Brazil nut (Bertholletia excelsa H.B.K.) prevents cognitive impairment in the offspring of obese mothers

Published online by Cambridge University Press:  12 February 2024

Lilian Fioravanso Apolinário
Affiliation:
Programa de Pós-Graduação em Ciências em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Amanda Tais Silva
Affiliation:
Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Andrielli Pompermayer Rosa
Affiliation:
Laboratórios Integrados de Pesquisas Químicas, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Cleber da Silva Oliveira
Affiliation:
Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Cleberson Lira
Affiliation:
Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
João Pedro Costa dos Santos Guerra
Affiliation:
Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Júlia Furtado Friedrich
Affiliation:
Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Letícia Queiroz Rosa
Affiliation:
Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Rodrigo Chelegão
Affiliation:
Embrapa Agrosilvipastoril, Sinop, MT, Brazil
Sílvia de Carvalho Campos Botelho
Affiliation:
Embrapa Agrosilvipastoril, Sinop, MT, Brazil
Valéria Dornelles Gindri Sinhorin
Affiliation:
Laboratórios Integrados de Pesquisas Químicas, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
Júlio Cezar de Oliveira
Affiliation:
Programa de Pós-Graduação em Ciências em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil Grupo de Pesquisa Programação Perinatal de Doenças Metabólicas, conceito DOHaD, Laboratório de Doenças Metabólicas e Cardiovasculares, Núcleo de Pesquisa e Apoio Didático em Saúde, Sinop, MT, Brazil
Nádia Aléssio Velloso*
Affiliation:
Programa de Pós-Graduação em Ciências em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil Núcleo de Pesquisa e Apoio Didático em Saúde, Universidade Federal de Mato Grosso (UFMT), Sinop, MT, Brazil
*
Corresponding author: N. A. Velloso; Email: na.velloso@gmail.com

Abstract

Maternal obesity may trigger long-term neurodevelopmental disorders in offspring. Considering the benefits of the Brazil nut (Bertholletia excelsa H.B.K.), a rich source of nutrients such as selenium, this study aimed to evaluate its effect on the behavior of obese rat offspring and its relationship with oxidative stress. From 60 days of age until weaning, female Wistar rats were fed a high-fat diet (mHF) or an HF diet supplemented with 5% Brazil nut (mHF/BN), while control mothers (mCTL) were fed a standard diet or a standard diet supplemented with 5% Brazil nut (mBN). Male pups received a standard diet throughout life and, at 30 and 90 days old, were subjected to behavioral tasks to evaluate anxiety and cognition. Biochemical evaluations were performed at 90 days of age. No alterations were observed in the anxiety behavior of the offspring. However, the offspring of the mHF group (oHF) exhibited impaired short-term memory at 30 and 90 days of age and impaired long-term memory at 30 days. Short-term memory impairment was prevented by Brazil nuts in young rats (30 days). While the serum selenium concentration was reduced in the oHF group, the serum catalase concentration was reduced in all groups, without changes in lipid peroxidation or protein carbonylation. Brazil nut maternal diet supplementation prevented short- and long-term cognitive impairment in the offspring, which may be related to the selenium levels.

Type
Original Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press in association with The International Society for Developmental Origins of Health and Disease (DOHaD)

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References

Segovia, SA, Vickers, MH, Gray, C, Reynolds, CM. Maternal obesity, inflammation, and developmental programming. BioMed Res Int. 2014; 2014, 114.CrossRefGoogle ScholarPubMed
Ross, MG, Desai, M. Developmental programming of offspring obesity, adipogenesis, and appetite. Clin Obstet Gynecol. 2013; 56(3), 529536.CrossRefGoogle ScholarPubMed
Batistuzzo, A, Ribeiro, MO. Clinical and subclinical maternal hypothyroidism and their effects on neurodevelopment, behavior and cognition. Arch Endocrinol Metab. 2020; 64(1), 8995.CrossRefGoogle ScholarPubMed
Gluckman, P, Hanson, M, Buklijas, T. A conceptual framework for the developmental origins of health and disease. J Dev Orig Health Dis. 2010; 1(1), 618.CrossRefGoogle ScholarPubMed
Howell, KR, Powell, TL. Effects of maternal obesity on placental function and fetal development. Reproduction. 2017; 153(3), 97108.CrossRefGoogle ScholarPubMed
Ojeda, ML, Nogales, F, Romero-Herrera, I, Carreras, O. Fetal programming is deeply related to maternal selenium status and oxidative balance; experimental offspring health repercussions. Nutrients. 2021; 13(6), 124.CrossRefGoogle ScholarPubMed
Tain, YL, Hsu, CN. Metabolic syndrome programming and reprogramming: mechanistic aspects of oxidative stress. Antioxidants (Basel). 2022; 11(11), 123.Google ScholarPubMed
Catalano, PM, Ehrenberg, HM. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG. 2006; 113(10), 11261133.CrossRefGoogle Scholar
Álvarez-Bueno, C, Cavero-Redondo, I, Lucas-de la Cruz, L, Notario-Pacheco, B, Martínez-Vizcaíno, V. Association between pre-pregnancy overweight and obesity and children’s neurocognitive development: a systematic review and meta-analysis of observational studies. Int J Epidemiol. 2017; 46(5), 16531666.CrossRefGoogle ScholarPubMed
Botelho, SCC, Baldoni, AB, Tonini, H, et al. Fruits, seeds and oil of Brazil nuts produced in Mato Grosso state. Floresta Ambiente. 2019; 26(2), 18.Google Scholar
Cardoso, BR, Duarte, GBS, Reis, BZ, Cozzolino, SMF. Brazil nuts: nutritional composition, health benefits and safety aspects. Food Res Int. 2017; 100, 918.CrossRefGoogle ScholarPubMed
Cominetti, C, Cozzolino, SMF. Funções plenamente reconhecidas de nutrientes Selênio, 2009. (Vol 8). International Life Sciences Institute do Brasil, São Paulo - SP - Brazil. pp. 320.Google Scholar
Silva Junior, EC, Wadt, LHO, Silva, KE, et al. Natural variation of selenium in Brazil nuts and soils from the Amazon region. Chemosphere. 2017; 188, 650658.CrossRefGoogle ScholarPubMed
Yang, J. Brazil nuts and associated health benefits: a review. LWT - food science and technology 2009, 42:15731580.CrossRefGoogle Scholar
Babür, E, Tan, B, Yousef, M, et al. Deficiency but not supplementation of selenium impairs the hippocampal long-term potentiation and hippocampus-dependent learning. Biol Trace Elem Res. 2019; 192(2), 252262.CrossRefGoogle Scholar
Nogueira, BSL, Ducatti, M, Horiquini-Barbosa, E. O consumo de selênio e sua relação com a manutenção da função cognitiva: uma revisão sistemática sobre humanos e animais. Rev Neurocienc. 2020; 28, 131.CrossRefGoogle Scholar
Martínez García, RM, Jiménez Ortega, AI, López Sobaler, AM, Ortega, RM. Nutrition strategies that improve cognitive function. Nutr Hosp. 2018; 7, 1619.Google Scholar
Theodore, LE, Kellow, NJ, McNeil, EA, et al. Nut consumption for cognitive performance: a systematic review. Adv Nutr. 2021; 12(3), 777792.CrossRefGoogle ScholarPubMed
Tan, BL, Norhaizan, ME. Effect of high-fat diets on oxidative stress, cellular inflammatory response and cognitive function. Nutrients. 2019; 11(11), 2579.CrossRefGoogle ScholarPubMed
Page, KC, Jones, EK, Anday, EK. Maternal and postweaning high-fat diets disturb hippocampal gene expression, learning, and memory function. Am J Physiol Regul Integr Comp Physiol. 2014; 306(8), R527537.CrossRefGoogle ScholarPubMed
Cordner, ZA, Khambadkone, SG, Boersma, GJ, et al. Maternal high-fat diet results in cognitive impairment and hippocampal gene expression changes in rat offspring. Exp Neurol. 2019; 318, 92100.CrossRefGoogle ScholarPubMed
Brasil. Regras para análises de sementes, 2009. Ministério da Agricultura, Pecuária e Abastecimento, Brasília – DF – Brazil. pp. 399.Google Scholar
Zenebon, O, Pascuet, NS, Tiglea, P. Métodos químicos e físicos para análises de alimentos, 2005. Instituto Adolfo Lutz, São Paulo – SP. pp. 1018.Google Scholar
Carioni, VMO. Desenvolvimento de procedimentos para determinação de As e Se em organismos marinhos por espectrometria de absorção atômica com geração de hidretos e amostragem de suspensão (SLS-HG AAS). Pós-Graduação em Ciência e Tecnologia/Química, Universidade Federal do ABC Paulista, Thesis of Master’s degree. 2010, 111.Google Scholar
Takino, M, Tanaka, T. Determination of aflatoxins in food by LC/MS/MS. Agilent Technologies. 2008, 18.Google Scholar
Pereira, LO. Protocolo de indução de obesidade em ratas a partir do perfil de ingestão alimentar de mulheres obesas brasileiras. Pós-Graduação em Biologia Funcional e Molecular, Universidade Estadual Campinas, Thesis of Master’s degree. 2002, 130.Google Scholar
Reeves, PG, Nielsen, FH, Fahey, GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American institute of nutrition ad Hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123(11), 19391951.CrossRefGoogle Scholar
Rayman, MP. Food-chain selenium and human health: emphasis on intake. Br J Nutr. 2008; 100(2), 254268.CrossRefGoogle ScholarPubMed
Hogan, C, Perkins, AV. Selenoproteins in the human placenta: how essential is selenium to a healthy start to life? Nutrients. 2022; 14(3), 118.CrossRefGoogle ScholarPubMed
Griebel, G, Rodgers, RJ, Perrault, G, Sanger, DJ. Risk assessment behaviour: evaluation of utility in the study of 5-HT-related drugs in the rat elevated plus-maze test. Pharmacol Biochem Behav. 1997; 57(4), 817827.Google Scholar
Cohen, H, Matar, MA, Joseph, Z. Animal models of posttraumatic stress disorder. Curr Protoc Neurosci. 2013; 64(1), 9 45 19 45 18.CrossRefGoogle Scholar
Ennaceur, A, Delacour, J. A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res. 1988; 31(1), 4759.CrossRefGoogle ScholarPubMed
Njung'e, K, Handley, SL. Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav. 1991; 38(1), 6367.CrossRefGoogle Scholar
Ohkawa, H, Ohishi, N, Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979; 95(2), 351358.CrossRefGoogle ScholarPubMed
Kohn, HI, Liversedge, M. On a new aerobic metabolite whose production by brain is inhibited by apomorphine, emetine, ergotamine, epinephrine, and menadione. J Pharmacol Exp Ther. 1944; 82, 292300.Google Scholar
Percario, S, Vital, A, Jablonka, F. Dosagem do malondialdeido. Newslab. 1994; 2, 4650.Google Scholar
Colombo, G, Clerici, M, Garavaglia, ME, et al. A step-by-step protocol for assaying protein carbonylation in biological samples. J Chromatogr B Analyt Technol Biomed Life Sci. 2016; 1019, 178190.CrossRefGoogle ScholarPubMed
Misra, HP, Fridovich, I. The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972; 247, 31703175.CrossRefGoogle Scholar
Nelson, DP, Kiesow, LA. Enthalphy of decomposition of hydrogen peroxide by catalase at 25 1C (with molar extinction coefficients of H2O2 solution in the UV). Anal Biochem. 1972; 49, 474478.CrossRefGoogle Scholar
Bradford, MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72(1-2), 248254.CrossRefGoogle Scholar
Gong, YY, Watson, S, Routledge, MN. Aflatoxin exposure and associated human health effects, a review of epidemiological studies. Food safety. 2016; 4(1), 1427.CrossRefGoogle ScholarPubMed
ANVISA. Resolution of director’s board – RDC number 07, 2011. https://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2011/res0007_18_02_2011_rep.html. Accessed June 14, 2022.Google Scholar
Sasaki, A, de Vega, WC, St-Cyr, S, Pan, P, McGowan, PO. Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience. 2013; 240, 112.CrossRefGoogle ScholarPubMed
Kang, SS, Kurti, A, Fair, DA, Fryer, JD. Dietary intervention rescues maternal obesity induced behavior deficits and neuroinflammation in offspring. J Neuroinflammation. 2014; 11(1), 112.CrossRefGoogle ScholarPubMed
Bellisario, V, Panetta, P, Balsevich, G, et al. Maternal high fat diet acts as a stressor increasing maternal glucocorticoids’ signaling to the fetus and disrupting maternal behavior and brain activation in C57BL/6J mice. Psychoneuroendodrinology. 2015; 50, 138150.CrossRefGoogle Scholar
Philpot, RM, Wecker, L. Dependence of adolescent novelty-seeking behavior on response phenotype and effects of apparatus scaling. Behav Neurosci. 2008; 122(4), 861875.CrossRefGoogle ScholarPubMed
Macri, S, Adriani, W, Chiarotti, F, Laviola, G. Risk taking during exploration of a plus-maze is greater in adolescent than in juvenile or adult mice. Anim Behav. 2002; 64(4), 541546.CrossRefGoogle Scholar
Stansfield, KH, Kirstein, CL. Effects of novelty on behavior in the adolescent and adult rat. Dev Psychobiol. 2006; 48(1), 1015.CrossRefGoogle ScholarPubMed
Graf, AE, Lallier, SW, Waidyaratne, G, et al. Maternal high fat diet exposure is associated with increased hepcidin levels, decreased myelination, and neurobehavioral changes in male offspring. Brain Behav Immun. 2016; 58, 369378.CrossRefGoogle ScholarPubMed
Janthakhin, Y, Rincel, M, Costa, AM, Darnaudéry, M, Ferreira, G. Maternal high fat diet leads to hippocampal and amygdala dendritic remodeling in adult male offspring. Psychoneuroendocrino. 2017; 83, 4957.CrossRefGoogle ScholarPubMed
Tozuka, Y, Wada, E, Wada, K. Diet-induced obesity in female mice leads to peroxidized lipid accumulations and impairment of hippocampal neurogenesis during the early life of their offspring. FASEB J. 2009; 23(6), 19201934.CrossRefGoogle ScholarPubMed
Hatanaka, Y, Wada, K, Kabuta, T. Maternal high fat diet leads to persistent synaptic instability in mouse offspring via oxidative stress during lactation. Neurochem Int. 2016; 97, 99108.CrossRefGoogle ScholarPubMed
Dias, CT, Curi, HT, Payolla, TB, et al. Maternal high fat diet stimulates proinflammatory pathway and increases the expression of tryptophan hydroxylase 2 (TPH2) and brain-derived neurotrophic factor (BDNF) in adolescent mice hippocampus. Neurochem Int. 2020; 139, 110.CrossRefGoogle ScholarPubMed
Bilbo, SD, Tsang, V. Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J. 2010; 24(6), 21042115.CrossRefGoogle ScholarPubMed
Sen, S, Simmons, RA. Maternal antioxidant supplementation prevents adiposity in the offspring of western diet-fed rats. Diabetes. 2010; 59(12), 30583065.CrossRefGoogle ScholarPubMed
Jiang, JT, Jiang, YJ. The influence of PHED in diet-induced obesity pregnant rats on offspring oxidative stress in liver. Eur Rev Med Pharmaco. 2018; 22, 24682476.Google ScholarPubMed
Moraes-Souza, RQ, Vesentini, G, Paula, VG, et al. Oxidative stress profile of mothers and their offspring after maternal consumption of high-fat diet in rodents: a systematic review and meta-analysis. Oxid Med Cell Longev. 2021; 2021, 118.CrossRefGoogle ScholarPubMed
Glorieux, C, Zamocky, M, Sandoval, JM, Verrax, J, Calderon, PB. Regulation of catalase expression in healthy and cancerous cells. Free Rad Biol Med. 2015; 87, 8497.CrossRefGoogle ScholarPubMed
Cardoso, BR, Apolinário, D, da Silva Bandeira, V, et al. Effects of Brazil nut consumption on selenium status and cognitive performance in older adults with mild cognitive impairment: a randomized controlled pilot trial. Eur J Nutr. 2016; 55(1), 107116.CrossRefGoogle Scholar
Pieczynska, J, Grajeta, H. The role of selenium in human conception and pregnancy. J Trace Elem Med Bio. 2015; 29, 3138.CrossRefGoogle ScholarPubMed
Labunskyy, VM, Hatfield, DL, Gladyshev, VN. Selenoproteins: molecular pathways and physiological roles. Physiol Rev. 2014; 94(3), 739777.CrossRefGoogle ScholarPubMed
Nogueira, CW, Barbosa, NV, Rocha, JBT. Toxicology and pharmacology of synthetic organoselenium compounds: an update. Arch Toxicol. 2021; 95(4), 11791226.CrossRefGoogle ScholarPubMed
Sievers, E, Arpe, T, Schleyerbach, U, Garbe-Schonberg, D, Schaub, J. Plasma selenium in preterm and term infants during the first 12 months of life. J Trace Elem Med Biol. 2001; 14(4), 218222.CrossRefGoogle ScholarPubMed
Dorea, JG. Selenium and breast-feeding. Br J Nutr. 2002; 88(5), 443461.CrossRefGoogle ScholarPubMed
Schramel, P, Hasse, S, Ovcar-Pavlu, J. Selenium, cadmium, lead, and mercury concentrations in human breast milk, in placenta, maternal blood, and the blood of the newborn. Biol Trace Elem Res. 1988; 15(1), 111124.CrossRefGoogle ScholarPubMed
Han, XJ, Xiao, YM, Ai, BM, et al. Effects of organic selenium on lead-induced impairments of spatial learning and memory as well as synaptic structural plasticity in rats. Biol Pharm Bull. 2014; 37(3), 466474.CrossRefGoogle ScholarPubMed
Amorós, R, Murcia, M, González, L, et al. Maternal selenium status and neuropsychological development in Spanish preschool children. Environ Res. 2018; 166, 215222.CrossRefGoogle ScholarPubMed
Schmutzler, C, Mentrup, B, Schomburg, L, Hoang-Vu, C, Herzog, V, Kohrle, J. Selenoproteins of the thyroid gland: expression, localization and possible function of glutathione peroxidase 3. Biol Chem. 2007; 388(10), 10531059.CrossRefGoogle ScholarPubMed
Cominetti, C, de Bortoli, MC, Garrido, AB Jr, Cozzolino, SM. Brazilian nut consumption improves selenium status and glutathione peroxidase activity and reduces atherogenic risk in obese women. Nutr Res. 2012; 32(6), 403407.CrossRefGoogle ScholarPubMed
Duarte, GBS, Reis, BZ, Rogero, MM, et al. Consumption of Brazil nuts with high selenium levels increased inflammation biomarkers in obese women: a randomized controlled trial. Nutrition. 2019; 63-64, 162168.CrossRefGoogle ScholarPubMed
Maranhão, PA, Kraemer-Aguiar, LG, de Oliveira, CL, et al. Brazil nuts intake improves lipid profile, oxidative stress and microvascular function in obese adolescents: a randomized controlled trial. Nutr Metab. 2011; 8, 18.CrossRefGoogle ScholarPubMed
Colpo, E, Vilanova, CD, Brenner Reetz, LG, et al. A single consumption of high amounts of the Brazil nuts improves lipid profile of healthy volunteers. J Nutr Metab. 2013; 2013, 17.CrossRefGoogle ScholarPubMed
Colpo, E, Vilanova, CDDA, Reetz, LGB, et al. Brazilian nut consumption by healthy volunteers improves inflammatory parameters. Nutrition. 2014; 30(4), 459465.CrossRefGoogle ScholarPubMed