Dietary intervention rescues maternal obesity induced behavior deficits and neuroinflammation in offspring
Open accessAbstract
Obesity induces a low-grade inflammatory state and has been associated with behavioral and cognitive alterations. Importantly, maternal environmental insults can adversely impact subsequent offspring behavior and have been linked with neurodevelopmental disorders such as autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (AHDH). It is unknown if maternal obesity significantly alters offspring sociability, a key ASD feature, and if altering maternal diet will provide an efficacious intervention paradigm for behavioral deficits. Here we investigated the impact of maternal high fat diet (HFD) and maternal dietary intervention during lactation on offspring behavior and brain inflammation in mice. We found that maternal HFD increased anxiety and decreased sociability in female offspring. Additionally, female offspring from HFD-fed dams also exhibited increased brain IL-1β and TNFα and microglial activation. Importantly, maternal dietary intervention during lactation was sufficient to alleviate social deficits and brain inflammation. Maternal obesity during gestation alone was sufficient to increase hyperactivity in male offspring, a phenotype that was not ameliorated by dietary intervention. These data suggest that maternal HFD acts as a prenatal/perinatal insult that significantly impacts offspring behavior and inflammation and that dietary intervention during lactation may be an easily translatable, efficacious intervention to offset some of these manifestations.
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In mice models, dietary intervention during pregnancy and lactation ameliorates the risk for obese mothers to have offspring with behavioral problems linked with autism.
“the finding in mice models that risk for obese mothers to have offspring with behavioral problems linked with autism is ameliorated by dietary intervention during pregnancy and lactation might be translatable to humans [262, 263].”
From The contribution of environmental exposure to the etiology of autism spectrum disorder (2019) · cites this paper as [262]
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An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Human gut microbes associated with obesity
Ley, R. E., Turnbaugh, P. J., Klein, S., & Gordon, J. I. (2006) · Nature · doi:10.1038/4441022a · Cited by 8,785 · see citing works
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823 · see citing works
Obesity alters gut microbial ecology
Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504978102 · Cited by 6,176 · see citing works
Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005) · Science · doi:10.1126/science.1110647 · Cited by 5,827 · see citing works
Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010.
Flegal, K., Carroll, M., Kit, B., & Ogden, C. (2012) · Journal of the American Medical Association (JAMA) · doi:10.1001/jama.2012.39 · Cited by 5,523 · see citing works
Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2
Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U., & Zoghbi, H. Y. (1999) · Nature Genetics · doi:10.1038/13810 · Cited by 4,990 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572 · see citing works
ATP mediates rapid microglial response to local brain injury in vivo
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., & Gan, W.-B. (2005) · Nature Neuroscience · doi:10.1038/nn1472 · Cited by 3,913 · see citing works
Guh, D. P., Zhang, W., Bansback, N., Amarsi, Z., Birmingham, C. L., & Anis, A. H. (2009) · BMC Public Health · doi:10.1186/1471-2458-9-88 · Cited by 3,855 · see citing works
Turnbaugh, P. J., Bäckhed, F., Fulton, L., & Gordon, J. I. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.02.015 · Cited by 2,915 · see citing works
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Neuroglial activation and neuroinflammation in the brain of patients with autism
Vargas, D. L., Nascimbene, C., Krishnan, C., Zimmerman, A. W., & Pardo, C. A. (2005) · Annals of Neurology · doi:10.1002/ana.20315 · Cited by 2,149 · cited 1× · see citing works
“Activation of microglia, the central nervous system (CNS) resident immune cells, often coincides with behavioral manifestations [14,42-45].”
BackgroundSemple, B. D., Blomgren, K., Gimlin, K., Ferriero, D. M., & Noble-Haeusslein, L. J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.04.001 · Cited by 2,132 · see citing works
Local self-renewal can sustain CNS microglia maintenance and function throughout adult life
Ajami, B., Bennett, J. L., Krieger, C., Tetzlaff, W., & Rossi, F. M. V. (2007) · Nature Neuroscience · doi:10.1038/nn2014 · Cited by 1,643 · see citing works
Maternal Immune Activation Alters Fetal Brain Development through Interleukin-6
Smith, S. E. P., Li, J., Garbett, K., Mirnics, K., & Patterson, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2178-07.2007 · Cited by 1,605 · see citing works
The Story of Rett Syndrome: From Clinic to Neurobiology
Chahrour, M., & Zoghbi, H. Y. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.001 · Cited by 1,265 · see citing works
Maternal Morbid Obesity and the Risk of Adverse Pregnancy Outcome
Cedergren, M. I. (2004) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000107291.46159.00 · Cited by 1,247 · see citing works
Microglia: new roles for the synaptic stripper
Kettenmann, H., Kirchhoff, F., & Verkhratsky, A. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.023 · Cited by 1,173 · see citing works
Has the Microbiota Played a Critical Role in the Evolution of the Adaptive Immune System?
Lee, Y. K., & Mazmanian, S. K. (2010) · Science · doi:10.1126/science.1195568 · Cited by 1,115 · see citing works
Microglial cell origin and phenotypes in health and disease
Saijo, K., & Glass, C. K. (2011) · Nature Reviews Immunology · doi:10.1038/nri3086 · Cited by 1,100 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
The core gut microbiome, energy balance and obesity
Turnbaugh, P. J., & Gordon, J. I. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.174136 · Cited by 993 · see citing works
The Role of Microglia in the Healthy Brain: Figure 1.
Tremblay, M.-È., Stevens, B., Sierra, A., Wake, H., Bessis, A., & Nimmerjahn, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4158-11.2011 · Cited by 992 · see citing works
Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children
Kang, D.-W., Park, J. G., Ilhan, Z. E., Wallstrom, G., LaBaer, J., Adams, J. B., & Krajmalnik-Brown, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068322 · Cited by 976 · see citing works
Maternal Infection Requiring Hospitalization During Pregnancy and Autism Spectrum Disorders
Atladóttir, H. Ó., Thorsen, P., Østergaard, L., Schendel, D. E., Lemcke, S., Abdallah, M., & Parner, E. T. (2010) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-1006-y · Cited by 916 · see citing works
Microglia: Scapegoat, saboteur, or something else?
Aguzzi, A., Barres, B. A., & Bennett, M. L. (2013) · Science · doi:10.1126/science.1227901 · Cited by 836 · see citing works
Elevated immune response in the brain of autistic patients
Li, X., Chauhan, A., Sheikh, A. M., Patil, S., Chauhan, V., Li, X.-M., Ji, L., Brown, T., & Malik, M. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.12.002 · Cited by 786 · see citing works
Gariepy, G., Nitka, D., & Schmitz, N. (2010) · International Journal of Obesity · doi:10.1038/ijo.2009.252 · Cited by 753 · see citing works
Tumor necrosis factor-α triggers a cytokine cascade yielding postoperative cognitive decline
Terrando, N., Monaco, C. G., Ma, D., Foxwell, B. M. J., Feldmann, M., & Maze, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014557107 · Cited by 730 · see citing works
Obesity in Pregnancy Stimulates Macrophage Accumulation and Inflammation in the Placenta
Challier, J. C., Basu, S., Bintein, T., Minium, J., Hotmire, K., Catalano, P. M., & Hauguel-de Mouzon, S. (2008) · Placenta · doi:10.1016/j.placenta.2007.12.010 · Cited by 712 · cited 1× · see citing works
“Notably, in humans, obese mothers have increased IL-6 in plasma and breast milk and increased IL-6 gene expression in placental macrophages [54-56].”
BackgroundMaternal Obesity and Risk of Preterm Delivery
Cnattingius, S., Villamor, E., Johansson, S., Bonamy, A. E., Persson, M., Wikström, A., & Granath, F. N. (2013) · JAMA · doi:10.1001/jama.2013.6295 · Cited by 701 · see citing works
Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders
Krakowiak, P., Walker, C. K., Bremer, A. A., Baker, A. S., Ozonoff, S., Hansen, R. L., & Hertz-Picciotto, I. (2012) · PEDIATRICS · doi:10.1542/peds.2011-2583 · Cited by 675 · see citing works
Sex differences in microglial colonization of the developing rat brain
Schwarz, J. M., Sholar, P. W., & Bilbo, S. D. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07630.x · Cited by 672 · see citing works
Malkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J., & Patterson, P. H. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.011 · Cited by 662 · see citing works
Wild-type microglia arrest pathology in a mouse model of Rett syndrome
Derecki, N. C., Cronk, J. C., Lu, Z., Xu, E., Abbott, S. B. G., Guyenet, P. G., & Kipnis, J. (2012) · Nature · doi:10.1038/nature10907 · Cited by 607 · see citing works
The immune system and developmental programming of brain and behavior
Bilbo, S. D., & Schwarz, J. M. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.08.006 · Cited by 579 · see citing works
Reynolds, R. M., Allan, K. M., Raja, E. A., Bhattacharya, S., McNeill, G., Hannaford, P. C., Sarwar, N., Lee, A. J., Bhattacharya, S., & Norman, J. E. (2013) · BMJ · doi:10.1136/bmj.f4539 · Cited by 571 · see citing works
Maternal High-Fat Diet Alters Methylation and Gene Expression of Dopamine and Opioid-Related Genes
Vucetic, Z., Kimmel, J. N., Totoki, K., Hollenbeck, E., & Reyes, T. M. (2010) · Endocrinology · doi:10.1210/en.2010-0505 · Cited by 556 · see citing works
Maternal infection and immune involvement in autism
Patterson, P. H. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2011.03.001 · Cited by 520 · 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
Fraser, A., Tilling, K., Macdonald-Wallis, C., Sattar, N., Brion, M.-J., Benfield, L., Ness, A., Deanfield, J., Hingorani, A., Nelson, S. M., et al. (2010) · Circulation · doi:10.1161/circulationaha.109.906081 · Cited by 486 · see citing works
Microbial contact during pregnancy, intestinal colonization and human disease
Rautava, S., Luoto, R., Salminen, S., & Isolauri, E. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.144 · Cited by 456 · see citing works
Depression and anxiety among US adults: associations with body mass index
Zhao, G., Ford, E. S., Dhingra, S., Li, C., Strine, T. W., & Mokdad, A. H. (2009) · International Journal of Obesity · doi:10.1038/ijo.2008.268 · Cited by 423 · see citing works
Activation of the maternal immune system induces endocrine changes in the placenta via IL-6
Hsiao, E. Y., & Patterson, P. H. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.12.017 · Cited by 402 · see citing works
Maternal obesity at conception programs obesity in the offspring
Shankar, K., Harrell, A., Liu, X., Gilchrist, J. M., Ronis, M. J. J., & Badger, T. M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00316.2007 · Cited by 385 · see citing works
Autism After Infection, Febrile Episodes, and Antibiotic Use During Pregnancy: An Exploratory Study
Atladóttir, H. Ó., Henriksen, T. B., Schendel, D. E., & Parner, E. T. (2012) · Pediatrics · doi:10.1542/peds.2012-1107 · Cited by 369 · see citing works
Neurogenesis, inflammation and behavior
Kohman, R. A., & Rhodes, J. S. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.003 · Cited by 363 · see citing works
Beumer, W., Gibney, S. M., Drexhage, R. C., Pont-Lezica, L., Doorduin, J., Klein, H. C., Steiner, J., Connor, T. J., Harkin, A., Versnel, M. A., et al. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.0212100 · Cited by 347 · see citing works
Crain, J. M., Nikodémová, M., & Watters, J. J. (2013) · Journal of Neuroscience Research · doi:10.1002/jnr.23242 · Cited by 335 · see citing works
Sullivan, E. L., Grayson, B. E., Takahashi, D. L., Robertson, N. D., Maier, A., Bethea, C. L., Smith, M. S., Coleman, K., & Grove, K. L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5560-09.2010 · Cited by 324 · see citing works
Elevation of Tumor Necrosis Factor-Alpha in Cerebrospinal Fluid of Autistic Children
Chez, M. G., Dowling, T., Patel, P. B., Khanna, P., & Kominsky, M. (2007) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2007.01.012 · Cited by 317 · cited 1× · see citing works
“Pro-inflammatory cytokines, including interleukin (IL)-1β and tumor necrosis factor (TNF)α, have been associated with increased anxiety, altered cognitive function [35-38], and are elevated in ASD patients [39-41].”
BackgroundRodriguez, A., Miettunen, J., Henriksen, T. B., Olsen, J., Obel, C., Taanila, A. M., Ebeling, H. E., Línnet, K., Moilanen, I., & Järvelin, M. (2007) · International Journal of Obesity · doi:10.1038/sj.ijo.0803741 · Cited by 282 · see citing works
Wohleb, E. S., Fenn, A. M., Pacenta, A. M., Powell, N. D., Sheridan, J. F., & Godbout, J. P. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.02.003 · Cited by 275 · see citing works
Microglia and Memory: Modulation by Early-Life Infection
Williamson, L. L., Sholar, P. W., Mistry, R. S., Smith, S. H., & Bilbo, S. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3688-11.2011 · Cited by 274 · see citing works
Collado, M. C., Laitinen, K., Salminen, S., & Isolauri, E. (2012) · Pediatric Research · doi:10.1038/pr.2012.42 · Cited by 270 · see citing works
Tozuka, Y., Kumon, M., Wada, E., Onodera, M., Mochizuki, H., & Wada, K. (2010) · Neurochemistry International · doi:10.1016/j.neuint.2010.05.015 · Cited by 260 · see citing works
Bilbo, S. D., Biedenkapp, J. C., Der-Avakian, A., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1748-05.2005 · Cited by 251 · cited 3× · see citing works
“This may be important since elevated CNS pro-inflammatory cytokines, including IL-1β and/or TNFα, have been associated with increased anxiety, decreased cognition, and altered social behaviors [35-38,62].”
BackgroundWhite, C. L., Pistell, P. J., Purpera, M. N., Gupta, S., Fernandez-Kim, S.-O., Hise, T. L., Keller, J. N., Ingram, D. K., Morrison, C. D., & Bruce-Keller, A. J. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.04.002 · Cited by 245 · see citing works
Barrientos, R. M., Hein, A. M., Frank, M. G., Watkins, L. R., & Maier, S. F. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2173-12.2012 · 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
Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood
Sasaki, A., de Vega, W. C., St-Cyr, S., Pan, P., & McGowan, P. O. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.02.044 · Cited by 194 · see citing works
Peripheral and central inflammation in autism spectrum disorders
Depino, A. M. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.10.003 · Cited by 189 · see citing works
Gestational obesity accentuates obesity in obesity-prone progeny
Levin, B. E., & Govek, E. K. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.4.r1374 · Cited by 179 · see citing works
Tozuka, Y., Wada, E., & Wada, K. (2009) · The FASEB Journal · doi:10.1096/fj.08-124784 · Cited by 177 · 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
A Longitudinal Study of Childhood Depression and Anxiety in Relation to Weight Gain
Rofey, D. L., Kolko, R. P., Iosif, A., Silk, J. S., Bost, J. E., Feng, W., Szigethy, E., Noll, R. B., Ryan, N. D., & Dahl, R. E. (2009) · Child Psychiatry & Human Development · doi:10.1007/s10578-009-0141-1 · Cited by 170 · see citing works
Maternal high-fat diet in mice programs emotional behavior in adulthood
Peleg-Raibstein, D., Luca, E., & Wolfrum, C. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.05.027 · Cited by 167 · 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
Misiak, B., Leszek, J., & Kiejna, A. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.08.003 · Cited by 136 · see citing works
Interleukin-1β Causes Anxiety by Interacting with the Endocannabinoid System
Rossi, S., Sacchetti, L., Napolitano, F., Chiara, V. D., Motta, C., Studer, V., Musella, A., Barbieri, F. R., Bari, M., Bernardi, G., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1515-12.2012 · Cited by 113 · see citing works
Maternal Obesity, Mode of Delivery, and Neonatal Outcome
Blomberg, M. (2013) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e318295657f · Cited by 94 · see citing works
Bralten, J., Franke, B., Waldman, I., Rommelse, N., Hartman, C., Asherson, P., Banaschewski, T., Ebstein, R. P., Gill, M., Miranda, A., et al. (2013) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.08.020 · Cited by 93 · see citing works
Dimmitt, R. A., Staley, E. M., Chuang, G. C., Tanner, S. M., Soltau, T. D., & Lorenz, R. G. (2010) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181e1a114 · Cited by 92 · see citing works
Yasui, D. H., Gonzales, M. L., Aflatooni, J. O., Crary-Dooley, F. K., Hu, D. J., Gavino, B. J., Golub, M. S., Vincent, J. B., Schanen, N. C., Olson, C. O., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt640 · Cited by 83 · see citing works
Maternal Obesity, Mode of Delivery, and Neonatal Outcome
Blomberg, M. (2014) · Obstetric Anesthesia Digest · doi:10.1097/01.aoa.0000452159.31332.e6 · Cited by 73 · see citing works
Odaka, Y., Nakano, M., Tanaka, T., Kaburagi, T., Yoshino, H., Sato‐Mito, N., & Sato, K. (2010) · Obesity · doi:10.1038/oby.2009.513 · Cited by 73 · see citing works
Maternal Obesity and Risk of Preterm Delivery
Cnattingius, S., Villamor, E., Johansson, S., Bonamy, A. K. E., Persson, M., Wikström, A.-K., & Granath, F. (2014) · Obstetric Anesthesia Digest · doi:10.1097/01.aoa.0000452160.31332.6b · Cited by 68 · see citing works
Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic
Sominsky, L., Walker, A. K., Ong, L. K., Tynan, R. J., Walker, F. R., & Hodgson, D. M. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.038 · Cited by 67 · see citing works
Lieshout, R. J. V. (2013) · Nutrition Reviews · doi:10.1111/nure.12059 · Cited by 67 · see citing works
Perinatal Maternal Fat Intake Affects Metabolism and Hippocampal Function in the Offspring
Walker, C., Naef, L., D’Asti, E., Long, H., Xu, Z., Moreau, A., & Azeddine, B. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1418.023 · Cited by 65 · see citing works
Hinkle, S. N., Sharma, A. J., Kim, S. Y., & Schieve, L. A. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.128 · Cited by 62 · see citing works
Desai, N., Roman, A., Rochelson, B. L., Gupta, M., Xue, X., Chatterjee, P. K., Tam, H. T., & Metz, C. N. (2013) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2013.05.001 · Cited by 58 · see citing works
Gender Differences in the Association Between Body Mass Index and Psychopathology
Desai, R. A., Manley, M. J., Desai, M. M., & Potenza, M. N. (2009) · CNS Spectrums · doi:10.1017/s1092852900023026 · Cited by 55 · see citing works
Correlation between maternal inflammatory markers and fetomaternal adiposity
Farah, N., Hogan, A. E., O’Connor, N., Kennelly, M., O'Shea, D. B., & Turner, M. J. (2012) · Cytokine · doi:10.1016/j.cyto.2012.05.024 · Cited by 45 · see citing works
Prenatal exposure to maternal obesity leads to hyperactivity in offspring
Fernandes, C., Grayton, H. M., Poston, L., Samuelsson, A.-M., Taylor, P. D., Collier, D. A., & Rodriguez, A. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.164 · Cited by 39 · see citing works
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Prenatal developmental origins of future psychopathology: mechanisms and pathways
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Cenit, M. C., Nuevo, I. C., Codoñer-Franch, P., Dinan, T. G., & Sanz, Y. (2017) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-017-0969-z · Cited by 163 · see citing works
Epigenetic Programming and Fetal Metabolic Programming
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Maternal body mass index before pregnancy as a risk factor for ADHD and autism in children
Andersen, C. H., Thomsen, P. H., Nohr, E. A., & Lemcke, S. (2018) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-017-1027-6 · Cited by 113 · see citing works
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Behavioral and transcriptomic analysis of Trem2-null mice: not all knockout mice are created equal
Kang, S. S., Kurti, A., Baker, K. E., Liu, C.-C., Colonna, M., Ulrich, J. D., Holtzman, D. M., Bu, G., & Fryer, J. D. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddx366 · Cited by 62 · see citing works
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- Authors
- Kang, S. S., Kurti, A., Fair, D. A., & Fryer, J. D.
- Affiliations
- Mayo Clinic in Florida (US)
- Oregon Health & Science University (US)
- Mayo Clinic (US)
- Corresponding author
- Fryer, John D
- Venue
- Journal of Neuroinflammation
- Published
- 2014-09-12
- Volume
- 11
- Issue
- 1
- Pages
- 156-156
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC4172780
- OpenAlex
- W2120666984
- Cited by
- 167
- References
- 86
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 18 · 2023: 6 · 2022: 20 · 2021: 20 · 2020: 15 · 2019: 17 · 2018: 14 · 2017: 14 · 2016: 12 · 2015: 7
- FWCI
- 10.35
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Mayo Foundation for Medical Education and Research
- GHR Foundation
- National Institutes of Health (MH091238, MH103632)
- Center for Individualized Medicine, Mayo Clinic
- National Institute of Mental Health (MH091238, R03MH103632, R00MH091238, R01MH096773, MH096773)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- maternal obesity, high-fat diet, lactation, offspring behavior, sociability, anxiety, hyperactivity, neuroinflammation, microglial activation, IL-1β, TNF-α, autism spectrum disorder, attention deficit hyperactivity disorder, neurodevelopmental disorders
- MeSH terms
- Animals, Behavior, Animal, Brain, Enzyme-Linked Immunosorbent Assay, Female, Immunohistochemistry, Inflammation, Lactation, Male, Mice, Inbred C57BL, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Mice, Diet, High-Fat, Real-Time Polymerase Chain Reaction
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