Microbiota signatures relating to reduced memory and exploratory behaviour in the offspring of overweight mothers in a murine model
Open accessAbstract
An elevated number of women of reproductive age are overweight, predisposing their offspring to metabolic and neuropsychiatric disorders. Gut microbiota is influenced by maternal factors, and has been implicated in the pathogenesis of neurodegenerative diseases. Our aim was to explore the effects of maternal high-fat feeding on the relationship linking gut microbiota and cognitive development in the offspring. Murine offspring born to dams undergoing normal diet (NDm) and high-fat diet (HFDm) were studied at 1 or 6 months of age to assess cognitive function by Y-maze test, cerebral glucose metabolism and insulin sensitivity by Positron Emission Tomography, brain density by Computed Tomography, microbiota profile (colon, caecum) and inferred metabolic pathways (KEGG analysis) by 16S ribosomal RNA sequencing. From 3 weeks post-weaning, mice born to HFDm developed hyperphagia and overweight, showing reduction in memory and exploratory behaviour, and brain insulin resistance in adulthood. We identified a panel of bacteria characterizing offspring born to HFD dams from early life, and correlating with dysfunction in memory and exploratory behaviour in adults (including Proteobacteria phylum, Parabacteroides and unclassified Rikenellaceae genera). Microbiota-derived metabolic pathways involved in fatty acid, essential aminoacid and vitamin processing, sulphur metabolism, glutaminergic activation and Alzheimer's disease were differently present in the HFDm and NDm offspring groups. Our results document tight relationships between gut dysbiosis and memory and behavioural impairment in relation to maternal HFD. Persistent bacterial signatures induced by maternal HFD during infancy can influence cognition during adulthood, opening the possibility of microbiota-targeted strategies to contrast cognitive decline.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Evidence from animal models suggests that the gut microbiota could be an underlying factor linking maternal diet to neurodevelopment.
“In recent years, evidence from animal models suggests that the gut microbiota could be an underlying factor linking maternal diet to neurodevelopment (244-246).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [244]
Investigations into the effect of high-fat or Western diets revealed that some diet-induced shifts in the microbial profile mediated behavioral and cognitive impairments in the offspring.
“Investigations into the effect of high-fat or Western diets revealed that some dietinduced shifts in the microbial profile mediated behavioral and cognitive impairments in the offspring (244-246),”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [244]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.6.593 · Cited by 20,391 · see citing works
Metagenomic biomarker discovery and explanation
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011) · Genome Biology · doi:10.1186/gb-2011-12-6-r60 · Cited by 16,192 · see citing works
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
Langille, M. G. I., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., Clemente, J. C., Burkepile, D. E., Vega Thurber, R. L., Knight, R., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2676 · Cited by 9,116 · see citing works
Quality control and preprocessing of metagenomic datasets
Schmieder, R., & Edwards, R. A. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr026 · Cited by 4,989 · see citing works
Gut microbiome alterations in Alzheimer’s disease
Vogt, N. M., Kerby, R. L., Dill-McFarland, K. A., Harding, S. J., Merluzzi, A. P., Johnson, S. C., Carlsson, C. M., Asthana, S., Zetterberg, H., Blennow, K., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-13601-y · Cited by 2,137 · see citing works
Monocyte chemoattractant protein 1 in obesity and insulin resistance
Sartipy, P., & Loskutoff, D. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1133870100 · Cited by 1,201 · see citing works
γ-Aminobutyric acid production by culturable bacteria from the human intestine
Barrett, E., Ross, R. P., O'Toole, P. W., Fitzgerald, G. F., & Stanton, C. (2012) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2012.05344.x · Cited by 1,156 · see citing works
Collado, M. C., Rautava, S., Aakko, J., Isolauri, E., & Salminen, S. (2016) · Scientific Reports · doi:10.1038/srep23129 · Cited by 1,098 · see citing works
Akbari, E., Asemi, Z., Daneshvar Kakhaki, R., Bahmani, F., Kouchaki, E., Tamtaji, O. R., Hamidi, G. A., & Salami, M. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00256 · Cited by 946 · see citing works
Samuelsson, A.-M., Matthews, P. A., Argenton, M., Christie, M. R., McConnell, J. M., Jansen, E. H. J. M., Piersma, A. H., Ozanne, S. E., Twinn, D. F., Remacle, C., et al. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.101477 · Cited by 923 · see citing works
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
Carnitine biosynthesis in mammals
Vaz, F. M., & Wanders, R. J. A. (2002) · Biochemical Journal · doi:10.1042/0264-6021:3610417 · Cited by 769 · see citing works
Tyrosine, Phenylalanine, and Catecholamine Synthesis and Function in the Brain2
Fernstrom, J. D., & Fernstrom, M. H. (2007) · The Journal of Nutrition · doi:10.1093/jn/137.6.1539s · Cited by 755 · see citing works
Chronic Glutamate Toxicity in Neurodegenerative Diseases—What is the Evidence?
Lewerenz, J., & Maher, P. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00469 · Cited by 721 · see citing works
Hypothalamic KATP channels control hepatic glucose production
Pocai, A., Lam, T. K. T., Gutierrez-Juarez, R., Obici, S., Schwartz, G. J., Bryan, J., Aguilar-Bryan, L., & Rossetti, L. (2005) · Nature · doi:10.1038/nature03439 · Cited by 645 · see citing works
The role of insulin receptor signaling in the brain
Plum, L., Schubert, M., & Brüning, J. C. (2005) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2005.01.008 · Cited by 604 · see citing works
Carnitine biosynthesis in mammals
Vaz, F. M., & Wanders, R. J. A. (2002) · Biochemical Journal · doi:10.1042/bj3610417 · Cited by 544 · see citing works
Bergström, A., Skov, T. H., Bahl, M. I., Roager, H. M., Christensen, L. B., Ejlerskov, K. T., Mølgaard, C., Michaelsen, K. F., & Licht, T. R. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00342-14 · Cited by 532 · see citing works
Enduring consequences of maternal obesity for brain inflammation and behavior of offspring
Bilbo, S. D., & Tsang, V. (2010) · The FASEB Journal · doi:10.1096/fj.09-144014 · Cited by 489 · see citing works
Altered Gut Microbiota in a Mouse Model of Alzheimer’s Disease
Zhang, L., Wang, Y., Xiayu, X., Shi, C., Chen, W., Song, N., Fu, X., Zhou, R., Xu, Y.-F., Huang, L., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170020 · Cited by 449 · see citing works
Ma, J., Prince, A., Bader, D., Hu, M., Ganu, R., Baquero, K. C., Blundell, P., Harris, R. A., Frias, A. E., Grove, K. L., et al. (2014) · Nature Communications · doi:10.1038/ncomms4889 · Cited by 440 · see citing works
Collado, M. C., Isolauri, E., Laitinen, K., & Salminen, S. (2010) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2010.29877 · Cited by 381 · see citing works
The early infant gut microbiome varies in association with a maternal high-fat diet
Chu, D. M., Antony, K. M., Ma, J., Prince, A., Showalter, L., Moller, M., & Aagaard, K. M. (2016) · Genome Medicine · doi:10.1186/s13073-016-0330-z · Cited by 377 · see citing works
Chang, G., Gaysinskaya, V. A., Karatayev, O., & LEIBOWITZ, S. F. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2642-08.2008 · Cited by 374 · see citing works
Regulation of Blood Glucose by Hypothalamic Pyruvate Metabolism
Lam, T. K. T., Gutierrez-Juarez, R., Pocai, A., & Rossetti, L. (2005) · Science · doi:10.1126/science.1112085 · Cited by 341 · see citing works
The role of maternal obesity in the risk of neuropsychiatric disorders
Rivera, H. M., Christiansen, K. J., & Sullivan, E. L. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00194 · Cited by 307 · see citing works
Percentage of Gestational Diabetes Mellitus Attributable to Overweight and Obesity
Kim, S. Y., England, L., Wilson, H. G., Bish, C., Satten, G. A., & Dietz, P. (2010) · American Journal of Public Health · doi:10.2105/ajph.2009.172890 · Cited by 302 · see citing works
Boix-Amorós, A., Collado, M. C., & Mira, A. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00492 · Cited by 283 · see citing works
Childhood mental ability and dementia
Whalley, L. J., Starr, J. M., Athawes, R. W. B., Hunter, D. C., Pattie, A., & Deary, I. J. (2000) · Neurology · doi:10.1212/wnl.55.10.1455 · Cited by 274 · see citing works
Laursen, M. F., Andersen, L. B. B., Michaelsen, K. F., Mølgaard, C., Trolle, E., Bahl, M. I., & Licht, T. R. (2016) · mSphere · doi:10.1128/msphere.00069-15 · Cited by 252 · see citing works
Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome
Dinan, T. G., & Cryan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.103 · Cited by 246 · see citing works
Bäuerl, C., Collado, M. C., Diaz Cuevas, A., Viña, J., & Pérez Martínez, G. (2018) · Letters in Applied Microbiology · doi:10.1111/lam.12882 · Cited by 238 · see citing works
Metabolism of endocannabinoids and related N ‐acylethanolamines: Canonical and alternative pathways
Ueda, N., Tsuboi, K., & Uyama, T. (2013) · FEBS Journal · doi:10.1111/febs.12152 · Cited by 235 · see citing works
Maternal pre‐pregnancy obesity and risk for inattention and negative emotionality in children
Rodriguez, A. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2009.02133.x · Cited by 233 · see citing works
Nivoit, P., Morens, C., Assche, F. A. V., Jansen, E. H. J. M., Poston, L., Remacle, C., & Reusens, B. (2009) · Diabetologia · doi:10.1007/s00125-009-1316-9 · Cited by 221 · see citing works
Obesity as a risk factor for Alzheimer's disease: weighing the evidence
Alford, S., Patel, D. K., Perakakis, N., & Mantzoros, C. S. (2017) · Obesity Reviews · doi:10.1111/obr.12629 · Cited by 219 · see citing works
Central Resistin Overexposure Induces Insulin Resistance Through Toll-Like Receptor 4
Benomar, Y., Gertler, A., Lacy, P. D., Crépin, D., Hamouda, H. O., Riffault, L., & Taouis, M. (2012) · Diabetes · doi:10.2337/db12-0237 · Cited by 197 · see citing works
Pre-pregnancy weight, gestational weight gain, and the gut microbiota of mothers and their infants
Stanislawski, M. A., Dabelea, D., Wagner, B. D., Sontag, M. K., Lozupone, C., & Eggesbø, M. Å. (2017) · Microbiome · doi:10.1186/s40168-017-0332-0 · Cited by 181 · see citing works
Maternal Obesity Is Associated with Alterations in the Gut Microbiome in Toddlers
Galley, J. D., Bailey, M. T., Dush, C. M. K., Schoppe‐Sullivan, S. J., & Christian, L. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113026 · Cited by 180 · see citing works
Parental Dietary Fat Intake Alters Offspring Microbiome and Immunity
Myles, I. A., Fontecilla, N. M., Janelsins, B., Vithayathil, P. J., Segre, J. A., & Datta, S. K. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301057 · Cited by 174 · see citing works
High fat diet‐induced maternal obesity alters fetal hippocampal development
Niculescu, M. D., & Lupu, D. S. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.08.005 · Cited by 162 · see citing works
Arachidonic Acid and the Brain
Rapoport, S. I. (2008) · Journal of Nutrition · doi:10.1093/jn/138.12.2515 · Cited by 157 · see citing works
Hinkle, S. N., Schieve, L. A., Stein, A. D., Swan, D. W., Ramakrishnan, U., & Sharma, A. J. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.143 · Cited by 153 · see citing works
Lemas, D. J., Young, B. E., Baker, P. R., Tomczik, A., Soderborg, T. K., Hernandez, T. L., de la Houssaye, B. A., Robertson, C. E., Rudolph, M. C., Ir, D., et al. (2016) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.126375 · Cited by 150 · see citing works
Nagpal, R., Tsuji, H., Takahashi, T., Kawashima, K., Nagata, S., Nomoto, K., & Yamashiro, Y. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01997 · Cited by 150 · see citing works
Dietary L-lysine and calcium metabolism in humans.
Civitelli, R., Villareal, D. T., Agnusdei, D., Nardi, P., Avioli, L. V., & Gennari, C. (1992) · PubMed · Cited by 149 · see citing works
Mueller, N. T., Shin, H., Pizoni, A., Werlang, I. C. R., Matte, Ú. D. S., Goldani, M. Z., Goldani, H. A. S., & Domínguez-Bello, M. G. (2016) · Scientific Reports · doi:10.1038/srep23133 · Cited by 141 · see citing works
Neuronal LRP1 Regulates Glucose Metabolism and Insulin Signaling in the Brain
Liu, C., Hu, J., Tsai, C., Yue, M., Melrose, H. L., Kanekiyo, T., & Bu, G. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5180-14.2015 · Cited by 140 · see citing works
Brion, M., Zeegers, M., Jaddoe, V. W. V., Verhulst, F. C., Tiemeier, H. W., Lawlor, D. A., & Smith, G. D. (2010) · PEDIATRICS · doi:10.1542/peds.2010-0651 · Cited by 138 · see citing works
Maternal Prepregnancy BMI and Child Cognition: A Longitudinal Cohort Study
Basatemür, E., GARDINER, J. S., Williams, C. L., Melhuish, E. C., Barnes, J., & Sutcliffe, A. G. (2012) · PEDIATRICS · doi:10.1542/peds.2012-0788 · Cited by 125 · see citing works
Page, K., Jones, E. K., & Anday, E. K. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00319.2013 · Cited by 118 · see citing works
Heni, M., Wagner, R., Kullmann, S., Gancheva, S., Roden, M., Peter, A., Stefan, N., Preissl, H., Häring, H.-U., & Fritsche, A. (2017) · Diabetes · doi:10.2337/db16-1380 · Cited by 115 · see citing works
Sanguinetti, E., Collado, M. C., Marrachelli, V. G., Monleón, D., Selma‐Royo, M., Pardo-Tendero, M., Burchielli, S., & Iozzo, P. (2018) · Scientific Reports · doi:10.1038/s41598-018-23261-1 · Cited by 115 · see citing works
Casas, M., Chatzi, L., Carsin, A., Amiano, P., Guxens, M., Kogevinas, M., Koutra, K., Lertxundi, N., Murcia, M., Rebagliato, M., et al. (2013) · International Journal of Epidemiology · doi:10.1093/ije/dyt002 · Cited by 114 · see citing works
The Impact of Prepregnancy Obesity on Children’s Cognitive Test Scores
Tanda, R., Salsberry, P. J., Reagan, P. B., & Fang, M. Z. (2012) · Maternal and Child Health Journal · doi:10.1007/s10995-012-0964-4 · Cited by 111 · see citing works
Torres-Espínola, F. J., Berglund, S. K., Garcia-Valdes, L., León, M. T. M., Jerez, A., Campos, D., Moreno‐Torres, R., Rueda, R., Catena, A., Pérez-Garcı́a, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133010 · Cited by 111 · see citing works
Epigenetic regulation of development by histone lysine methylation
Dambacher, S., Hahn, M., & Schotta, G. (2010) · Heredity · doi:10.1038/hdy.2010.49 · Cited by 108 · see citing works
Dash, S., Xiao, C., Morgantini, C., Koulajian, K., & Lewis, G. F. (2015) · Diabetes · doi:10.2337/db14-0685 · Cited by 108 · see citing works
Ramnanan, C. J., Saraswathi, V., Smith, M. S., Donahue, E. P., Farmer, B., Farmer, T. D., Neal, D. W., Williams, P. E., Lautz, M., Mari, A., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci45472 · Cited by 94 · see citing works
Schmidt‐Wilcke, T., Poljansky, S., Hierlmeier, S., Hausner, J., & Ibach, B. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.04.092 · Cited by 89 · see citing works
Santos, V. D., Thomann, P. A., Wüstenberg, T., Seidl, U., Essig, M., & Schröder, J. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100156 · Cited by 73 · see citing works
Han, J., Xu, J., Epstein, P. N., & Liu, Y. Q. (2005) · Diabetologia · doi:10.1007/s00125-005-1854-8 · Cited by 70 · see citing works
Lépinay, A. L., Larrieu, T., Joffre, C., Acar, N., Gárate, I., Castanon, N., Ferreira, G., Goustard, B., Guesnet, P., Brétillon, L., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.12.008 · Cited by 66 · see citing works
Microbiome to Brain: Unravelling the Multidirectional Axes of Communication
Aidy, S. E., Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-20215-0_15 · Cited by 64 · see citing works
Makizako, H., Shimada, H., Doi, T., Park, H., Yoshida, D., Uemura, K., Tsutsumimoto, K., Liu-Ambrose, T. Y. L., & Suzuki, T. (2013) · BMC Neurology · doi:10.1186/1471-2377-13-102 · Cited by 60 · see citing works
Crosstalk between Gut Microbiota and Central Nervous System: A Focus on Alzheimer's Disease
Junges, V. M., Closs, V. E., Nogueira, G., & Gottlieb, M. G. V. (2018) · Current Alzheimer Research · doi:10.2174/1567205015666180904155908 · Cited by 58 · see citing works
Mental Ability in Childhood and Cognitive Aging
Gow, A. J., Johnson, W., Pattie, A., Whiteman, M. C., Starr, J. M., & Deary, I. J. (2008) · Gerontology · doi:10.1159/000118098 · Cited by 57 · see citing works
Shimazu, S., & Miklya, I. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2003.11.016 · Cited by 57 · see citing works
Wang, J., Ye, F., Cheng, X., Zhang, X., Liu, F., Liu, G., Ni, M., Qiao, S., Zhou, W., & Zhang, Y. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160138 · Cited by 52 · see citing works
Neurocognitive development in preterm infants: Insights from different approaches
Mento, G., & Bisiacchi, P. S. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.08.008 · Cited by 50 · see citing works
The effects of excess amino acids on maintenance of pregnancy and fetal growth in rats.
Shuji, M., & NIIYAMA, Y. (1982) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.28.557 · Cited by 35 · see citing works
Chen, H., Simar, D., & Morris, M. J. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12623 · Cited by 33 · see citing works
Decreased basal insulin secretion from pancreatic islets of pups in a rat model of maternal obesity
Zambrano, E., Sosa-Larios, T. C., Calzada, L., Ibáñez, C. A., Mendoza-Rodríguez, C. A., Morales, A., & Morimoto, S. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0321 · Cited by 32 · see citing works
Sanguinetti, E., Guzzardi, M. A., Panetta, D., Tripodi, M., Sena, V. D., Quaglierini, M., Burchielli, S., Salvadori, P. A., & Iozzo, P. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00188 · Cited by 32 · see citing works
Sanguinetti, E., Liistro, T., Mainardi, M., Pardini, S., Salvadori, P. A., Vannucci, A., Burchielli, S., & Iozzo, P. (2016) · Diabetologia · doi:10.1007/s00125-015-3848-5 · Cited by 20 · see citing works
Velloso, L. A. (2012) · Endocrinology · doi:10.1210/en.2011-2077 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
Berding, K., Vlckova, K., Marx, W., Schellekens, H., Stanton, C., Clarke, G., Jacka, F., Dinan, T. G., & Cryan, J. F. (2021) · Advances in Nutrition · doi:10.1093/advances/nmaa181 · Cited by 451 · see citing works
The impact of maternal high-fat diet on offspring neurodevelopment
Urbonaite, G., Knyzeliene, A., Bunn, F. S., Smalskys, A., & Neniškytė, U. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.909762 · Cited by 118 · see citing works
Agranyoni, O., Meninger-Mordechay, S., Uzan-Yulzari, A., Oren, Z., Salmon‐Divon, M., Rodin, D., Raz, O., Koman, I. E., Koren, O., Pinhasov, A., et al. (2021) · npj Biofilms and Microbiomes · doi:10.1038/s41522-021-00193-9 · Cited by 73 · see citing works
Guzzardi, M. A., Ederveen, T. H. A., Rizzo, F. M., Weisz, A., Collado, M. C., Muratori, F., Gross, G., Alkema, W. B. L., & Iozzo, P. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.12.009 · Cited by 69 · see citing works
Unravelling the impacts of western-style diets on brain, gut microbiota and cognition
Kendig, M. D., Leigh, S., & Morris, M. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.031 · Cited by 60 · see citing works
The impact of maternal obesity on childhood neurodevelopment
Tong, L., & Kalish, B. T. (2020) · Journal of Perinatology · doi:10.1038/s41372-020-00871-0 · Cited by 59 · see citing works
Leblic, B. C., Selma‐Royo, M., Collado, M. C., Abril, N., & García‐Barrera, T. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c02622 · Cited by 52 · see citing works
Infant gut microbiota contributes to cognitive performance in mice
Cerdó, T., Ruiz-Rodriguez, A., Acuña, I., Torres-Espínola, F. J., Menchén-Márquez, S., Gámiz, F., Gallo, M., Jehmlich, N., Haange, S., von Bergen�, M., et al. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2023.11.004 · Cited by 53 · see citing works
An examination of maternal prenatal BMI and human fetal brain development
Norr, M. E., Hect, J. L., Lenniger, C. J., van den Heuvel, M. P., & Thomason, M. E. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13301 · Cited by 47 · see citing works
The Molecular Gut-Brain Axis in Early Brain Development
Muhammad, F., Fan, B., Wang, R., Ren, J., Jia, S., Wang, L., Chen, Z., & Liu, X. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315389 · Cited by 47 · see citing works
Early-Life Environment Influence on Late-Onset Alzheimer’s Disease
Gauvrit, T., Benderradji, H., Buée, L., Blum, D. L., & Vieau, D. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.834661 · Cited by 42 · see citing works
Davis, J. M., & Mire, E. (2021) · Brain and Neuroscience Advances · doi:10.1177/23982128211003484 · Cited by 39 · see citing works
Malnutrition and the microbiome as modifiers of early neurodevelopment
Coley, E. J. L., & Hsiao, E. Y. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.06.004 · Cited by 40 · see citing works
Selenium supplementation influences mice testicular selenoproteins driven by gut microbiota
Ramírez‐Acosta, S., Selma‐Royo, M., Collado, M. C., Navarro, F., Abril, N., & García‐Barrera, T. (2022) · Scientific Reports · doi:10.1038/s41598-022-08121-3 · Cited by 40 · see citing works
Avolio, E., Olivito, I., Rosina, E., Romano, L., Angelone, T., Bartolo, A. D., Scimeca, M., Bellizzi, D., D’Aquila, P., Passarino, G., et al. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.038 · Cited by 40 · see citing works
Wang, M., Zhang, Y., Miller, D., Rehman, N., Cheng, X., Yeo, J., Joe, B., & Hill, J. W. (2020) · Endocrinology · doi:10.1210/endocr/bqz041 · Cited by 36 · see citing works
Ramírez, V., González-Palacios, P., Baca, M. Á., González-Domenech, P., Fernández-Cabezas, M., Álvarez-Cubero, M. J., Rodrigo, L. S., & Rivas, A. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.158219 · Cited by 36 · see citing works
Hassib, L., de Oliveira, C. L., Rouvier, G. A., Kanashiro, A., Guimarães, F. S., & Ferreira, F. R. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2226282 · Cited by 33 · see citing works
Tsan, L., Sun, S., Hayes, A., Bridi, L., Chirala, L., Noble, E. E., Fodor, A. A., & Kanoski, S. E. (2021) · Nutritional Neuroscience · doi:10.1080/1028415x.2021.1980697 · Cited by 29 · see citing works
Out of our skull, in our skin: the Microbiota-Gut-Brain axis and the Extended Cognition Thesis
Boem, F., Ferretti, G., & Caiani, S. Z. (2021) · Biology & Philosophy · doi:10.1007/s10539-021-09790-6 · Cited by 28 · see citing works
Imaging of brain glucose uptake by PET in obesity and cognitive dysfunction: life-course perspective
Iozzo, P., & Guzzardi, M. A. (2019) · Endocrine Connections · doi:10.1530/ec-19-0348 · Cited by 24 · see citing works
Renson, A., Kasselman, L. J., Dowd, J. B., Waldron, L., Jones, H. E., & Herd, P. (2020) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2020.100155 · Cited by 18 · see citing works
More than just a number: the gut microbiota and brain function across the extremes of life
Nuzum, N. D., Deady, C., Kittel‐Schneider, S., Cryan, J. F., O’Mahony, S. M., & Clarke, G. A. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2418988 · Cited by 20 · see citing works
The influence of maternal diet on offspring’s gut microbiota in early life
Peng, L., Tan, Y., & Bajinka, O. (2023) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-023-07305-0 · Cited by 15 · see citing works
Gureev, A. P., Syromyatnikov, M., Ignatyeva, D. A., Valuyskikh, V. V., Solodskikh, S. A., Panevina, A. V., Vladimirovna, G. M., Kokina, A. V., & Popov, V. N. (2020) · PLoS ONE · doi:10.1371/journal.pone.0241784 · Cited by 15 · see citing works
Guzzardi, M. A., Rosa, F. L., Granziera, F., Panetta, D., Pardo-Tendero, M., Barone, M., Turroni, S., Faita, F., Kusmic, C., Brigidi, P., et al. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.08.009 · Cited by 14 · see citing works
Guzzardi, M. A., Rosa, F. L., Campani, D., Insilla, A. C., Sena, V. D., Panetta, D., Brunetto, M. R., Bonino, F., Collado, M. C., & Iozzo, P. (2021) · Nutrients · doi:10.3390/nu13103438 · Cited by 13 · see citing works
Structural and functional neuroimaging of the effects of the gut microbiome
Montoro, R. A., Singh, A. P., & Yu, J. J. (2022) · European Radiology · doi:10.1007/s00330-021-08486-5 · Cited by 12 · see citing works
Probiotic Lactobacilli Ameliorate Antibiotic-Induced Cognitive and Behavioral Impairments in Mice
Рашидовна, Я. Д., Novoselova, V., Alexandrova, A., Arslanova, A., Yakovleva, O. V., Shaidullov, I. F., Nikolaev, Y. A., El-Registan, G. I., Кудрин, В. С., & Ситдикова, Г. Ф. (2024) · Microbiology Research · doi:10.3390/microbiolres15030099 · Cited by 11 · see citing works
Sometti, D., Ballan, C., Wang, H., Braun, C., & Enck, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-83994-4 · Cited by 10 · see citing works
Quoilin, C., Amadieu, C., Fievez, F., Delzenne, N. M., de Timary, P., Duqué, J., & Leclercq, S. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109384 · Cited by 8 · see citing works
The gut microbiome and psycho-cognitive traits
Vernice, N. A., Shah, N. B., Lam, E. H., Herd, P., Reiss, A. B., & Kasselman, L. J. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.08.014 · Cited by 7 · see citing works
Oh, J. K., Vasquez, R., Hwang, I., Oh, Y. N., Kim, S., Kang, S. H., Joung, J. Y., Oh, N. S., Kim, S., Yoon, Y., et al. (2021) · Microorganisms · doi:10.3390/microorganisms9091908 · Cited by 7 · see citing works
Obesity and Cognitive Function: Leptin Role Through Blood–Brain Barrier and Hippocampus
Al-Suhaimi, E. A., Rubaish, A. A., Al-Dossary, H. A., Homeida, M. A., Shehzad, A., & Homeida, A. M. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05262-0 · Cited by 6 · see citing works
Insulin and IGF signaling in the brain: multilevel regulation of synaptic and network homeostasis
Li, L., He, H., & Wang, Y. (2026) · Frontiers in Endocrinology · doi:10.3389/fendo.2026.1793536 · Cited by 5 · see citing works
Zhang, C., Yu, Y., Yue, L., Chen, Y., Chen, Y., Liu, Y., Guo, C., Su, Q., & Xiang, Z. (2025) · Communications Biology · doi:10.1038/s42003-025-07538-6 · Cited by 5 · see citing works
Gkintoni, E., Papachatzi, E., Efthymiadou, E., Magriplis, E., & Vantarakis, A. (2025) · Healthcare · doi:10.3390/healthcare13202653 · Cited by 4 · see citing works
Guzzardi, M. A., Collado, M. C., Panetta, D., Tripodi, M., & Iozzo, P. (2022) · Metabolites · doi:10.3390/metabo12090828 · Cited by 4 · see citing works
Schade, R., Song, L., Cordner, Z. A., Ding, H., Peterson, D. A., Moran, T. H., Tamashiro, K. L., & Serre, C. B. D. L. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113987 · Cited by 3 · see citing works
Guo, X., Zhao, Y., Pan, Y., Huang, J., Wang, Z., Li, P., Yuan, W., He, Y., Qiu, J., Dong, J., et al. (2025) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2025.10.021 · Cited by 2 · see citing works
Ding, L., Yang, S., Wu, F., Pilling, D., Zhang, J., Pool, K., Nishvanthi, M., Babington, S., Maloney, S. K., Chen, L., et al. (2026) · Microbiome · doi:10.1186/s40168-025-02332-2 · Cited by 1 · see citing works
Merle, L., Rastelli, M., Datiche, F., Véjux, A., Jacquin, A., Bouret, S. G., & Bénani, A. (2025) · Neuroendocrinology · doi:10.1159/000543499 · Cited by 1 · see citing works
Microbiota intestinal: su importancia en la salud y los factores que la modifican
Espinoza, Y. R. (2020) · Latin American Journal of Clinical Sciences and Medical Technology · doi:10.34141/ljcs3995284
Economic Insecurity: Meaning and Measurement
Mughan, A. (2006) · The Knowledge Bank (The Ohio State University)
Efecto de la obesidad sobre la memoria y el aprendizaje
Martínez, C., & Torres‐Fernández, O. (2023) · Biosalud · doi:10.17151/biosa.2019.18.2.6
- Authors
- Sanguinetti, E., Guzzardi, M. A., Tripodi, M., Panetta, D., Selma-Royo, M., Zega, A., Telleschi, M., Collado, M. C., & Iozzo, P.
- Affiliations
- Scuola Superiore Sant'Anna (IT)
- Istituto di Fisiologia Clinica (IT)
- Corresponding author
- Iozzo, Patricia
- ORCID
- Venue
- Scientific Reports
- Published
- 2019-08-30
- Volume
- 9
- Issue
- 1
- Pages
- 12609-12609
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6717200
- OpenAlex
- W2971014020
- Cited by
- 45
- References
- 76
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 5 · 2022: 10 · 2021: 11 · 2020: 8 · 2019: 1
- FWCI
- 2.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Horizon 2020 Framework Programme
- FP7 Health (278603)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- maternal high-fat diet, gut microbiota, offspring cognitive function, memory impairment, exploratory behavior, hyperphagia, brain insulin resistance, brain glucose metabolism, gut dysbiosis, Parabacteroides, Rikenellaceae, Proteobacteria, Alzheimer's disease, sulfur metabolism, maternal obesity, brain development
- MeSH terms
- Gastrointestinal Microbiome, Animals, Cognition, Disease Models, Animal, Exploratory Behavior, Female, Humans, Insulin Resistance, Memory, Mother-Child Relations, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Maternal Nutritional Physiological Phenomena, Overweight, Mice, Diet, High-Fat
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review