Palabras clave
Anxiety
Depression
Microbiota
High-fat high-sugar diet Estrés vital temprano
Ansiedad
Depresión
Microbiota
Dieta rica en grasas y azúcares
Cómo citar
Resumen
Antecedentes: El estrés temprano (ET) y el consumo materno de una dieta alta en grasas y azúcares (HFS) pueden tener efectos perjudiciales sobre las respuestas emocionales en la adultez. La microbiota y el eje intestino-cerebro podrían mediar la regulación del estrés y las emociones. Método: Ratas macho jóvenes se expusieron a separación materna (SM) y a consumo materno y postnatal de una dieta HFS (45%kcal grasa saturada, 17%kcal sacarosa). Se evaluó el comportamiento ansioso mediante el laberinto cero elevado y el comportamiento depresivo mediante natación forzada y preferencia por sacarosa. Se analizó la microbiota en heces empleando cromatografía de gas y espectrometría de masas. Resultados: La exposición combinada a la SM y el consumo de una dieta HFS revirtió parcialmente la ansiedad y depresión en adultos causadas independientemente por cada factor adverso. La dieta influyó negativamente más que la exposición a ET en la microbiota y ambos factores modificaron su composición contrarrestando parcialmente sus efectos negativos. Conclusiones: Los efectos del ET y una dieta HFS por independiente varían con respecto a los efectos de la combinación de ambos factores, sugiriendo que el ET y la dieta interactúan modulando en el adulto la respuesta al estrés y la microbiota intestinal.
Citas
Abenavoli, L., Scarpellini, E., Colica, C., Boccuto, L., Salehi, B., Sharifi-Rad, J., Aiello, V., Romano, B., De Lorenzo, A., Izzo, A. A., & Capasso, R. (2019). Gut microbiota and obesity: A role for probiotics. Nutrients, 11(11), Article 2690. https://doi.org/10.3390/nu11112690
Adan, R.A.H., van der Beek, E.M., Buitelaar, J.K., Cryan, J.F., Hebebrand, J., Higgs, S., Schellekens, H., & Dickson, S.L., (2019). Nutritional psychiatry: Towards improving mental health by what you eat. European Neuropsychopharmacology, 29(12), 1321–1332. https://doi.org/10.1016/j. euroneuro.2019.10.011
Agorastos, A., Pervanidou, P., Chrousos, G.P., & Baker, D.G. (2019). Developmental trajectories of early life stress and trauma: A narrative review on neurobiological aspects beyond stress system dysregulation. Frontiers in Psychiatry, 10, Article 118. https://doi.org/10.3389/fpsyt.2019.00118
Anyan, J., & Amir, S. (2018). Too depressed to swim or too afraid to stop? A reinterpretation of the forced swim test as a measure of anxiety-like behavior. Neuropsychopharmacology, 43, 931–933. https://doi.org/10.1038/ NPP.2017.260
Armario, A. (2021). The forced swim test: Historical, conceptual and methodological considerations and its relationship with individual behavioral traits. Neuroscience and Biobehavioral Reviews, 128, 74–86. https://doi.org/10.1016/j.neubiorev.2021.06.014
Aslani, S., Vieira, N., Marques, F., Costa, P.S., Sousa, N., & Palha, J.A. (2015). The effect of high-fat diet on rat’s mood, feeding behavior and response to stress. Translational Psychiatry, 5(11), Article e684. https://doi.org/10.1038/ tp.2015.178
Bokulich, N.A., Subramanian, S., Faith, J.J., Gevers, D., Gordon, J.I., Knight, R., Mills, D.A., & Caporaso, J.G. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10, 57–59. https://doi.org/10.1038/nmeth.2276
Cao, B., Wang, J., Zhang, X., Yang, X., Poon, D.C.-H., Jelfs, B., Chan, R.H.M., Wu, J.C.-Y., & Li, Y., (2016). Impairment of decision making and disruption of synchrony between basolateral amygdala and anterior cingulate cortex in the maternally separated rat. Neurobiol. Learning & Memory, 136, 74–85. https://doi.org/10.1016/j.nlm.2016.09.015
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pẽa, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., & Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336. https://doi.org/10.1038/ nmeth.f.303
Chen, L.P., Murad, M.H., Paras, M.L., Colbenson, K.M., Sattler, A.L., Goranson, E.N., Elamin, M.B., Seime, R.J., Shinozaki, G., Prokop, L.J., & Zirakzadeh, A. (2010). Sexual abuse and lifetime diagnosis of psychiatric disorders: Systematic review and meta-analysis. Mayo Clinic Proceedings, 85, 618–629. https://doi.org/10.4065/mcp.2009.0583
Commons, K.G., Cholanians, A.B., Babb, J.A., & Ehlinger, D.G. (2017). The rodent forced swim test measures stress-coping strategy, not depression- like behavior. ACS Chemical Neuroscience, 8(5), 955–960. https://doi. org/10.1021/acschemneuro.7b00042
Cryan, J.F., O’riordan, K.J., Cowan, C.S.M., Sandhu, K. V., Bastiaanssen, T.F.S., Boehme, M., Codagnone, M.G., Cussotto, S., Fulling, C., Golubeva, A. V., Guzzetta, K.E., Jaggar, M., Long-Smith, C.M., Lyte, J.M., Martin, J.A., Molinero-Perez, A., Moloney, G., Morelli, E., Morillas, E., O’connor, R., Cruz-Pereira, J.S., Peterson, V.L., Rea, K., Ritz, N.L., Sherwin, E., Spichak, S., Teichman, E.M., van de Wouw, M., Ventura-Silva, A.P., Wallace-Fitzsimons, S.E., Hyland, N., Clarke, G., & Dinan, T.G. (2019). The microbiota-gut-brain axis. Physiological Reviews, 99(4), 1877–2013. https://doi.org/10.1152/physrev.00018.2018
Daniels, W.M.U., Pietersen, C.Y., Carstens, M.E., & Stein, D.J. (2004). Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metabolical Brain Disease, 19(1-2), 3–14. https://doi.org/10.1023/b:mebr.0000027412.19664.b3
de la Cuesta-Zuluaga, J., Mueller, N.T., Álvarez-Quintero, R., Velásquez- Mejía, E.P., Sierra, J.A., Corrales-Agudelo, V., Carmona, J.A., Abad, J.M., & Escobar, J.S. (2019). Higher fecal short-chain fatty acid levels are associated with gut microbiome dysbiosis, obesity, hypertension and cardiometabolic disease risk factors. Nutrients, 11(1), 51. https://doi. org/10.3390/nu11010051
Edgar, R.C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998. https://doi.org/10.1038/ nmeth.2604
Enqi, W., Jingzhu, S., Lingpeng, P., & Yaqin, L. (2021). Comparison of the gut microbiota disturbance in rat models of irritable bowel syndrome induced by maternal separation and multiple early-life adversity. Frontiers in Cellular and Infection Microbiology, 10, Article 581974. https://doi.org/10.3389/ fcimb.2020.581974
Fernandes, D.J., Spring, S., Roy, A.R., Qiu, L.R., Yee, Y., Nieman, B.J., Lerch, J.P., & Palmert, M.R. (2021). Exposure to maternal high-fat diet induces extensive changes in the brain of adult offspring. Translational Psychiatry, 11(1), Article 149. https://doi.org/10.1038/s41398-021-01274-1
Francis, H., & Stevenson, R. (2013). The longer-term impacts of Western diet on human cognition and the brain. Appetite, 63, 119-128. https://doi.org/10.1016/j.appet.2012.12.018
González-Pardo, H., Arias, J.L., Gómez-Lázaro, E., Taboada, I.L., & Conejo, N.M. (2020). Sex-specific effects of early life stress on brain mitochondrial function, monoamine levels and neuroinflammation. Brain Sciences, 10, 1–17. https://doi.org/10.3390/brainsci10070447
Haas, B.J., Gevers, D., Earl, A.M., Feldgarden, M., Ward, D. V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S.K., Sodergren, E., Methé, B., DeSantis, T.Z., Petrosino, J.F., Knight, R., & Birren, B.W. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494–504. https://doi.org/10.1101/ gr.112730.110
Johnson, S.A., Javurek, A.B., Painter, M.S., Murphy, C.R., Conard, C.M., Gant, K.L., Howald, E.C., Ellersieck, M.R., Wiedmeyer, C.E., Vieira- Potter, V.J., & Rosenfeld, C.S. (2017). Effects of a maternal high-fat diet on offspring behavioral and metabolic parameters in a rodent model. Journal of Developmental Origins of Health and Disease, 8(1), 75–88. https://doi.org/10.1017/S2040174416000490
Karl, P.J., Hatch, A.M., Arcidiacono, S.M., Pearce, S.C., Pantoja-Feliciano, I.G., Doherty, L.A., & Soares, J.W. (2018). Effects of psychological, environmental and physical stressors on the gut microbiota. Frontiers in Microbiology, 9, Article 2013. https://doi.org/10.3389/fmicb.2018.02013
Lippmann, M., Bress, A., Nemeroff, C.B., Plotsky, P.M., & Monteggia, L.M. (2007). Long-term behavioural and molecular alterations associated with maternal separation in rats. European Journal of Neuroscience, 25, 3091– 3098. https://doi.org/10.1111/j.14609568.2007.05522.x
Liu, R. T., Walsh, R. F. L., & Sheehan, A. E. (2019). Prebiotics and probiotics for depression and anxiety: A systematic review and meta-analysis of controlled clinical trials. Neuroscience and biobehavioral reviews, 102, 13–23. https://doi.org/10.1016/j.neubiorev.2019.03.023
López-Taboada, I., González-Pardo, H., & Conejo, N. M. (2020). Western diet: implications for brain function and behavior. Frontiers in Psychology, 11, Article 564413. https://doi.org/10.3389/fpsyg.2020.564413
Magoč, T., & Salzberg, S.L. (2011). FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27, 2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Malesza, I.J., Malesza, M., Walkowiak, J., Mussin, N., Walkowiak, D., Aringazina, R., Bartkowiak-Wieczorek, J., & Mądry, E. (2021). High- fat, western-style diet, systemic inflammation, and gut microbiota: A narrative review. Cells, 10(11), Article 3164. https://doi.org/10.3390/cells10113164
Maniam, J., Antoniadis, C.P., Le, V., & Morris, M.J. (2016). A diet high in fat and sugar reverses anxiety-like behaviour induced by limited nesting in male rats: Impacts on hippocampal markers. Psychoneuroendocrinology, 68, 202–209. https://doi.org/10.1016/j.psyneuen.2016.03.007
Maniam, J., & Morris, M.J. (2010). Palatable cafeteria diet ameliorates anxiety and depression-like symptoms following an adverse early environment. Psychoneuroendocrinology, 35, 717–728. https://doi.org/10.1016/j. psyneuen.2009.10.013
Moris, G., Arboleya, S., Mancabelli, L., Milani, C., Ventura, M., de los Reyes- Gavilán, C.G., & Gueimonde, M. (2018). Fecal microbiota profile in a group of myasthenia gravis patients. Scientific Reports, 8(1), Article 14384. https://doi.org/10.1038/s41598-018-32700-y
Morris, M.J., Beilharz, J.E., Maniam, J., Reichelt, A.C., & Westbrook,
R.F. (2015). Why is obesity such a problem in the 21st century? The intersection of palatable food, cues and reward pathways, stress, and cognition. Neuroscience and Biobehavioral Reviews, 58, 36–45. https://doi. org/10.1016/j.neubiorev.2014.12.002
Nemeroff, C.B. (2016). Paradise lost: The neurobiological and clinical consequences of child abuse and neglect. Neuron, 89, 892–909. https://doi.org/10.1016/j.neuron.2016.01.019
O’Mahony, S.M., McVey Neufeld, K.A., Waworuntu, R. V., Pusceddu, M.M., Manurung, S., Murphy, K., Strain, C., Laguna, M.C., Peterson, V.L., Stanton, C., Berg, B.M., Dinan, T.G., & Cryan, J.F. (2020). The enduring effects of early-life stress on the microbiota–gut–brain axis are buffered by dietary supplementation with milk fat globule membrane and a prebiotic blend. European Journal of Neuroscience, 51, 1042–1058. https://doi.org/10.1111/ejn.14514
Oriach, C.S., Robertson, R.C., Stanton, C., Cryan, J.F., & Dinan, T.G. (2016). Food for thought: The role of nutrition in the microbiota-gut-brain axis. Clinical Nutrition Experimental, 6, 25-35. https://doi.org/10.1016/j. yclnex.2016.01.003
Paulson, J.N., Colin Stine, O., Bravo, H.C., & Pop, M. (2013). Differential abundance analysis for microbial marker-gene surveys. Nature Methods, 10, 1200–1202. https://doi.org/10.1038/nmeth.2658
Pini, R.T.B., Ferreira do Vales, L.D.M., Braga Costa, T.M., & Almeida, S.S. (2017). Effects of cafeteria diet and high fat diet intake on anxiety, learning and memory in adult male rats. Nutritional Neuroscience, 20, 396–408. https://doi.org/10.1080/1028415x.2016.1149294
Porsolt, R.D., Bertin, A., & Jalfre, M. (1978). “Behavioural despair” in rats and mice: Strain differences and the effects of imipramine. European Journal of Pharmacology, 51, 291–294. https://doi.org/10.1016/0014-2999(78)90414-4
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F.O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(Database issue), D590-D596. https://doi.org/10.1093/nar/gks1219
Rabasa, C., Winsa-Jörnulf, J., Vogel, H., Babaei, C.S., Askevik, K., & Dickson,
S.L. (2016). Behavioral consequences of exposure to a high fat diet during the post-weaning period in rats. Hormones and Behavior, 85, 56–66. https:// doi.org/10.1016/j.yhbeh.2016.07.008
Rincel, M., Aubert, P., Chevalier, J., Grohard, P.A., Basso, L., Monchaux de Oliveira, C., Helbling, J.C., Lévy, É., Chevalier, G., Leboyer, M., Eberl, G., Layé, S., Capuron, L., Vergnolle, N., Neunlist, M., Boudin, H., Lepage, P., & Darnaudéry, M. (2019). Multi-hit early life adversity affects gut microbiota, brain and behavior in a sex-dependent manner. Brain, Behavior, and Immunity, 80, 179–192. https://doi.org/10.1016/j.bbi.2019.03.006
Rincel, M., Lépinay, A.L., Delage, P., Fioramonti, J., Théodorou, V.S., Layé, S., & Darnaudéry, M. (2016). Maternal high-fat diet prevents developmental programming by early-life stress. Translational Psychiatry, 6(11), Article e966. https://doi.org/10.1038/tp.2016.235
Rincel, M., Lépinay, A.L., Janthakhin, Y., Soudain, G., Yvon, S., Da Silva, S., Joffre, C., Aubert, A., Séré, A., Layé, S., Theodorou, V., Ferreira, G., & Darnaudéry, M. (2018). Maternal high-fat diet and early life stress differentially modulate spine density and dendritic morphology in the medial prefrontal cortex of juvenile and adult rats. Brain Structure and Function, 223, 883–895. https://doi.org/10.1007/s00429-017-1526-8
Rincel, M., Olier, M., Minni, A., de Oliveira, C.M., Matime, Y., Gaultier, E., Grit, I., Helbling, J.C., Costa, A.M., Lépinay, A., Moisan, M.P., Layé, S., Ferrier, L., Parnet, P., Theodorou, V., & Darnaudéry, M. (2019). Pharmacological restoration of gut barrier function in stressed neonates partially reverses long-term alterations associated with maternal separation. Psychopharmacology (Berlin), 236, 1583–1596. https://doi.org/10.1007/ s00213-019-05252-w
Romaní-Pérez, M., Lépinay, A.L., Alonso, L., Rincel, M., Xia, L., Fanet, H., Caillé, S., Cador, M., Layé, S., Vancassel, S., & Darnaudéry, M. (2017). Impact of perinatal exposure to high-fat diet and stress on responses to nutritional challenges, food-motivated behaviour and mesolimbic dopamine function. International Journal of Obesity, 41, 502–509. https://doi.org/10.1038/ijo.2016.236
Salazar, N., González, S., Nogacka, A.M., Rios-Covián, D., Arboleya, S., Gueimonde, M., & de los Reyes-Gavilán, C.G. (2019). Microbiome: Effects of ageing and diet. Current Issues in Molecular Biology, 36, 33–62. https:// doi.org/10.21775/cimb.036.033
Sasaki, A., de Vega, W., Sivanathan, S., St-Cyr, S., & McGowan, P. (2014). Maternal high-fat diet alters anxiety behavior and glucocorticoid signaling in adolescent offspring. Neuroscience, 272, 92–101. https://doi.org/10.1016/j. neuroscience.2014.04.012
Sasaki, A., de Vega, W.C., St-Cyr, S., Pan, P., & McGowan, P.O. (2013). Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience, 240, 1–12. https://doi.org/10.1016/j. neuroscience.2013.02.044
Scheggi, S., De Montis, M.G., & Gambarana, C. (2018). Making sense of rodent models of anhedonia. The International Journal of Psychopharmacology, 21(11), 1049-1065 https://doi.org/10.1093/ijnp/pyy083
Shepherd, J.K., Grewal, S.S., Fletcher, A., Bill, D.J., & Dourish, C.T. (1994). Behavioural and pharmacological characterisation of the elevated “zero- maze” as an animal model of anxiety. Psychopharmacology (Berlin), 116, 56–64. https://doi.org/10.1007/BF02244871
Silva, Y.P., Bernardi, A., & Frozza, R.L. (2020). The role of short-chain fatty acids from gut microbiota in gut-brain communication. Frontiers in Endocrinology (Lausanne), 11, Article 25. https://doi.org/10.3389/ fendo.2020.00025
Souto, T. dos S., Nakao, F.S.N., Giriko, C.Á., Dias, C.T., Cheberle,
A.I. do P., Lambertucci, R.H., & Mendes-da-Silva, C. (2020). Lard- rich and canola oil-rich high-fat diets during pregnancy promote rats’ offspring neurodevelopmental delay and behavioral disorders. Physiology & Behavior, 213, Article 112722. https://doi.org/10.1016/j.physbeh.2019.112722
Tsan, L., Décarie-Spain, L., Noble, E.E., & Kanoski, S.E. (2021). Western diet consumption during development: setting the stage for neurocognitive dysfunction. Frontiers in Neuroscience, 15, Article 632312. https://doi.org/10.3389/fnins.2021.632312
van Bodegom, M., Homberg, J.R., & Henckens, M.J.A.G. (2017). Modulation of the hypothalamic-pituitary-adrenal axis by early life stress exposure. Frontiers in Cellular Neuroscience, 11, Article 87. https://doi.org/10.3389/ fncel.2017.00087
van de Wouw, M., Boehme, M., Lyte, J.M., Wiley, N., Strain, C., O’Sullivan, O., Clarke, G., Stanton, C., Dinan, T.G., & Cryan, J.F. (2018). Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain–gut axis alterations. Journal of Physiology, 596, 4923–4944. https://doi.org/10.1113/ JP276431
Wang, D., Levine, J.L.S., Avila-Quintero, V., Bloch, M., & Kaffman, A. (2020). Systematic review and meta-analysis: effects of maternal separation on anxiety-like behavior in rodents. Translational Psychiatry, 10(1), Article 174. https://doi.org/10.1038/s41398-020-0856-0
Wang, S., Huang, M., You, X., Zhao, J., Chen, L., Wang, L., Luo, Y., & Chen, Y. (2018). Gut microbiota mediates the anti-obesity effect of calorie restriction in mice. Scientific Reports, 8(1), Article 13037. https://doi.org/10.1038/s41598-018-31353-1
Winther, G., Elfving, B., Müller, H.K., Lund, S., & Wegener, G. (2018). Maternal high-fat diet programs offspring emotional behavior in adulthood. Neuroscience, 388, 87–101. https://doi.org/10.1016/j.neuroscience.2018.07.014
Yang, Y., Duan, C., Huang, L., Xia, X., Zhong, Z., Wang, B., Wang, Y., & Ding, W. (2020). Juvenile high–fat diet–induced senescent glial cells in the medial prefrontal cortex drives neuropsychiatric behavioral abnormalities in mice. Behavioural Brain Research, 395, Article 112838. https://doi.org/10.1016/j.bbr.2020.112838