The DOI matches its Crossref record; 86 of the 86 references it cites were found in a registry or an index.
Maternal immune activation: Implications for neuropsychiatric disorders
Open accessAbstract
Epidemiological evidence implicates maternal infection as a risk factor for autism spectrum disorder and schizophrenia. Animal models corroborate this link and demonstrate that maternal immune activation (MIA) alone is sufficient to impart lifelong neuropathology and altered behaviors in offspring. This Review describes common principles revealed by these models, highlighting recent findings that strengthen their relevance for schizophrenia and autism and are starting to reveal the molecular mechanisms underlying the effects of MIA on offspring. The role of MIA as a primer for a much wider range of psychiatric and neurologic disorders is also discussed. Finally, the need for more research in this nascent field and the implications for identifying and developing new treatments for individuals at heightened risk for neuroimmune disorders are considered.
Overview
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
Verification
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?
In the citing paper
“Current MIA ASD models expose developing rodent pups to bacterial or viral mimetics [126] to elicit strong immune responses.”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [126]
In the citing paper
“MIA can be induced experimentally via immunogens, such as polyinosinic-polycytidylic acid (poly(I:C)) and lipopolysaccharide (LPS).”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [29]
In the citing paper
“MIA-induced disruption may work in a manner similar in directionality to rare highly penetrant ASD mutations, and may act as ‘priming’27, 28, 29, 30 or fetal programming21, 22 mechanisms that enhance risk of later developing ASD.”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [29]
In the citing paper
“Alterations of the host immune responses by gut microbiota are closely linked to ASD-related symptoms.”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [65]
In the citing paper
“The implicated cytokine pathways include, and not limited to, IL-5, IL-15, IL-17, IL-17a, IL-10, IL-1b, TNF-α, TGF-β1 and IFNγ [12, 18, 65, 66].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [65]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,951
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283
Schizophrenia risk from complex variation of complement component 4
Sekar, A., Bialas, A. R., de Rivera, H., Davis, A., Hammond, T. R., Kamitaki, N., Tooley, K., Presumey, J., Baum, M., Van Doren, V., et al. (2016) · Nature · doi:10.1038/nature16549 · Cited by 2,394
Genetic relationship between five psychiatric disorders estimated from genome-wide SNPs
Cross-Disorder Group of the Psychiatric Genomics Consortium (2013) · Nature Genetics · doi:10.1038/ng.2711 · Cited by 2,263
Abnormal neural oscillations and synchrony in schizophrenia
Uhlhaas, P. J., & Singer, W. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2774 · Cited by 2,120
Zika Virus and Birth Defects — Reviewing the Evidence for Causality
Rasmussen, S. A., Jamieson, D. J., Honein, M. A., & Petersen, L. R. (2016) · New England Journal of Medicine · doi:10.1056/nejmsr1604338 · Cited by 1,989
Evolution of the immune system in humans from infancy to old age
Simon, A. K., Hollander, G. A., & McMichael, A. (2015) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2014.3085 · Cited by 1,796
Trends in the prevalence of developmental disabilities in US children, 1997-2008
Boyle, C. A., Boulet, S., Schieve, L. A., Cohen, R. A., Blumberg, S. J., Yeargin-Allsopp, M., Visser, S., & Kogan, M. D. (2011) · Pediatrics · doi:10.1542/peds.2010-2989 · Cited by 1,732
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
The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring
Choi, G. B., Yim, Y. S., Wong, H., Kim, S., Kim, H., Kim, S. V., Hoeffer, C. A., Littman, D. R., & Huh, J. R. (2016) · Science · doi:10.1126/science.aad0314 · Cited by 1,214
Flagged first, then by citations
Cited by
Sorted by citations
Items 301–400 of 1,000
Antonson, A. M., Balakrishnan, B., Radlowski, E. C., Petr, G. T., & Johnson, R. W. (2018) · Developmental Neuroscience · doi:10.1159/000486850 · Cited by 38
Weber‐Stadlbauer, U., & Meyer, U. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.02.006 · Cited by 32
Page, N. F., Gandal, M. J., Estes, M. L., Cameron, S., Buth, J. E., Parhami, S., Ramaswami, G., Murray, K. D., Amaral, D. G., de Water, J. V., et al. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.10.016 · Cited by 35
Self-citationHughes, H. K., Onore, C. E., Careaga, M., Rogers, S. J., & Ashwood, P. (2022) · Brain Sciences · doi:10.3390/brainsci12020220 · Cited by 36
“Maternal inflammation during gestation confers an increased risk of ASD in the child and IL-6 has been implicated in ASD animal models of maternal infection and immune activation [11,52,53].”
BackgroundDecoding microRNAs in autism spectrum disorder
Li, J., Xu, X., Liu, J., Zhang, S., Tan, X., Li, Z., Zhang, J., & Wang, Z. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.11.005 · Cited by 40
A single-cell genomic atlas for maturation of the human cerebellum during early childhood
Ament, S. A., Cortes-Gutierrez, M., Herb, B. R., Mocci, E., Colantuoni, C., & McCarthy, M. M. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.ade1283 · Cited by 35
Hirotsu, A., Iwata, Y., Tatsumi, K., Miyai, Y., Matsuyama, T., & Tanaka, T. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172682 · Cited by 35
Deckmann, I., Santos‐Terra, J., Fontes‐Dutra, M., Rockenbach, M. K., Bauer‐Negrini, G., Schwingel, G. B., Riesgo, R. D. S., Bambini-Júnior, V., & Gottfried, C. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10137 · Cited by 36
“In fact, maternal immune activation (MIA) contributes to the onset of several neuropsychiatric disorders, including ASD (Estes & McAllister, 2016).”
BackgroundNeurodevelopmental disorders, immunity, and cancer are connected
Nussinov, R., Tsai, C., & Jang, H. (2022) · iScience · doi:10.1016/j.isci.2022.104492 · Cited by 35
“The impact of perturbations of the immune system during neurodevelopment (Estes and McAllister, 2016; Knuesel et al., 2014) emphasize the vital importance of the inter-relationships and their underlying mechanisms.”
Lampiasi, N., Bonaventura, R., Deidda, I., Zito, F., & Russo, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032703 · Cited by 39
Persistent Inflammation in Cerebral Palsy: Pathogenic Mediator or Comorbidity? A Scoping Review
Paton, M. C. B., Finch‐Edmondson, M., Dale, R. C., Fahey, M. C., Nold‐Petry, C. A., Nold, M. F., Griffin, A. R., & Novak, I. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11247368 · Cited by 34
“Not to mention, the confounding role of aberrant inflammation following perinatal infection and neonatal sepsis in CP [40,41], as well as maternal immune activation [42] and congenital abnormalities [43].”
BackgroundHu, Y., Hong, X.-Y., Yang, X., Ma, R.-H., Wang, X., Zhang, J., Feng, Q., Li, X., Sun, D., Li, X. M., et al. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.02.020 · Cited by 35
Li, Y., Zhang, X., & Li, Y. (2019) · CNS Spectrums · doi:10.1017/s1092852919001603 · Cited by 33
“Maternal immune activation (MIA) during pregnancy induces a dysregulated immune system in offspring and also leads to ASD-related phenotypes that persist well into adulthood.(60,61) Therefore,MIA has been widely used for inducing an animal model of ASD.”
BackgroundTargeted drug delivery for maternal and perinatal health: Challenges and opportunities
Sharma, A., Sah, N., Kannan, S., & Kannan, R. M. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113950 · Cited by 35
Chamera, K., Szuster-Głuszczak, M., Trojan, E., & Basta-Kaim, A. (2020) · Cells · doi:10.3390/cells9071676 · Cited by 31
“Those changes include increased susceptibility to adverse postnatal psychological outcomes, such as cognitive impairments and psychiatric disorders [1].”
BackgroundSherer, M. L., Lei, J., Creisher, P. S., Jang, M., Reddy, R., Voegtline, K., Olson, S., Littlefield, K. E., Park, H.-S., Ursin, R. L., et al. (2021) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2021.03.028 · Cited by 34
“detrimental to long-term fetal and neonatal outcomes.(2,10,11) We assayed cytokine mRNA expression during SARS-CoV-2 infection as a biomarker for inflammation.”
BackgroundZhou, J., Tong, J., Ru, X., Teng, Y., Geng, M., Yan, S., Tao, F., & Huang, K. (2023) · BMC Medicine · doi:10.1186/s12916-023-03173-2 · Cited by 34
“Animal models show that maternal immune activation-induced inflammatory processes have important negative effects on neuroplasticity and neurogenesis and are sufficient to impart lifelong psychiatric and neurologic disorders in offspring [21, 22].”
BackgroundMaternal viral infection causes global alterations in porcine fetal microglia
Antonson, A. M., Lawson, M. A., Caputo, M. P., Matt, S. M., Leyshon, B. J., & Johnson, R. W. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817014116 · Cited by 34
“Although swine do have TH17 cells that produce IL-17a (57, 58), plasma IL-17a was not impacted by PRRSV infection at the times sampled, suggesting that translation of maternal inflammatory signaling to the fetal brain may not include IL-17a in our model (59).”
BackgroundBadihian, N., Daniali, S. S., & Kelishadi, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.018 · Cited by 33
Mental health dished up—the use of iPSC models in neuropsychiatric research
McNeill, R. V., Ziegler, G. C., Radtke, F., Nieberler, M., Lesch, K., & Kittel‐Schneider, S. (2020) · Journal of Neural Transmission · doi:10.1007/s00702-020-02197-9 · Cited by 32
Goh, J.-Y., O’Sullivan, S. E., Shortall, S. E., Zordan, N., Piccinini, A. M., Potter, H. G., Fone, K. C. F., & King, M. V. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.05.076 · Cited by 33
“Crucially it appears that even subclinical MIA can increase vulnerability of the offspring to a second hit, thus increasing the likelihood of environmental stressors causing a schizophrenia- or ASD-like phenotype (Estes and McAllister, 2016).”
BackgroundLi, Y., Tang, J., Shu, Y., Peng, Y., Liu, Y., Meng, Y., Ping, Z., Xiao, H., & Yixiao, F. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.02.020 · Cited by 32
Steen, N. E., Rahman, Z., Szabó, A., Hindley, G., Parker, N., Cheng, W., Lin, A., O’Connell, K. S., Sheikh, M. A., Shadrin, A. A., et al. (2023) · Schizophrenia Bulletin · doi:10.1093/schbul/sbad082 · Cited by 34
“76–78 While microglia is the main innate immune cell in the brain with established neurodevelopmental and homeostatic functions, lymphocytes are also demonstrated in the developing brain at least partly involving their bidirectional interaction with microglia cells.”
Maternal prenatal infection and anxiety predict neurodevelopmental outcomes in middle childhood
O'Connor, T. G., Ciesla, A. A., Sefair, A. V., Thornburg, L. L., Brown, A. S., Glover, V., & O'Donnell, K. J. (2022) · Journal of Psychopathology and Clinical Science · doi:10.1037/abn0000746 · Cited by 31
“A prevailing model was that pregnancy was an immunosuppressive state and that a successful pregnancy was dependent on a shift to a Th2/anti-in fl ammatory response, although research has considered a wide array of pro-and anti-in fl ammatory cytokines such as interleukin(IL)-6, IL-17 or TNF-alpha (Estes & McAllister, 20…”
Antonson, A. M., Kenney, A. D., Chen, H. J., Corps, K. N., Yount, J. S., & Gur, T. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.05.004 · Cited by 33
Medial prefrontal cortex circuitry and social behaviour in autism
Mediane, D. H., Basu, S., Cahill, E., & Anastasiades, P. G. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110101 · Cited by 36
Balan, S., Toyoshima, M., & Yoshikawa, T. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.04.021 · Cited by 31
Zhao, Y., Liang, X., Zhu, F., Wen, Y. F., Xu, J., Yang, J., Ding, M., Cheng, B., Ma, M., Zhang, L., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.10.005 · Cited by 31
“Using rodent and non-human primate animal models, researchers have clearly demonstrated a causal relationship between maternal infection and autism spectrum disorder as well as SCZ related behavioral abnormalities (Estes and Mcallister, 2016).”
Jyonouchi, H., Geng, L., Rose, S., Bennuri, S. C., & Frye, R. E. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00071 · Cited by 34
The Role of Immune Factors in Shaping Fetal Neurodevelopment
Lu-Culligan, A., & Iwasaki, A. (2020) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-021120-033518 · Cited by 32
“…(MIA; see the sidebar titled Maternal Immune Activation) has now been implicated in a broad range of distinct disorders in offspring, and an outsized proportion of these are, strikingly, brain pathologies long suspected to have developmental origins (Estes & McAllister 2016, Knuesel et al. 2014).”
BackgroundCritical Role of the Maternal Immune System in the Pathogenesis of Autism Spectrum Disorder
Ravaccia, D., & Ghafourian, T. (2020) · Biomedicines · doi:10.3390/biomedicines8120557 · Cited by 32
“This association between the maternal immune system and ASD was first proposed following the 1960s Rubella outbreak, where the incidence of autism among children born to infected mothers increased substantially [20,21].”
BackgroundInfluentialIshihara, Y., Honda, T., Ishihara, N., Namba, K., Taketoshi, M., Tominaga, Y., Tsuji, M., Vogel, C. F. A., Yamazaki, T., Itoh, K., et al. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02559-y · Cited by 31
“C motif chemokine ligand 3; ChIP: Chromatin immunoprecipitation; DG: Dentate gyrus; GABA: Gamma-aminobutyric acid; GFAP: Glial fibrillary acidic protein; IHC: Immunohistochemistry; MIA: Maternal immune activation; OPC: Oligodendrocyte precursor cell; VPA: Valproic acid; VSD: Voltage-sensitive dye.”
BackgroundInfluentialDutra, M. L., Dias, P., Freiberger, V., Ventura, L., Comim, C. M., Martins, D. F., & Bobinski, F. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136974 · Cited by 33
A comprehensive approach to modeling maternal immune activation in rodents
Bucknor, M. C., Gururajan, A., Dale, R. C., & Hofer, M. J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1071976 · Cited by 37
Wang, Y., Chen, Y., Zhou, Q., Xu, J., Qian, Q., Ni, P., & Qian, Y. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00222 · Cited by 32
“Neurodegeneration is characterized by neuronal dysfunction and death in the central nervous system (CNS) (Estes and McAllister, 2016).”
BackgroundInfluentialImmunogenetics of autism spectrum disorder: A systematic literature review
Arenella, M., Matulevičiūtė, R., Tamouza, R., Leboyer, M., McAlonan, G. M., Bralten, J., & Murphy, D. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.09.010 · Cited by 37
“Also, due to their effects on the maternal-fetal interface, variations in HLA class I genes may modulate the previously established link between maternal immune (over)activation and neurodevelopment conditions, including ASD and schizophrenia (Estes & McAllister, 2016; Scola & Duong, 2017).”
Prenatal Nutritional Factors and Neurodevelopmental Disorders: A Narrative Review
Cernigliaro, F., Santangelo, A., Nardello, R., Cascio, S. L., D’Agostino, S., Correnti, E., Marchese, F., Pitino, R., Valdese, S., Rizzo, C., et al. (2024) · Life · doi:10.3390/life14091084 · Cited by 39
“Therefore, an hyperactivation of the immune system at this stage could cause deleterious effects on brain development, leading to disorders such as epilepsy, schizophrenia, Parkinson’s disease, Alzheimer’s disease, and ASD [37].”
BackgroundMaldonado‐Ruiz, R., Garza‐Ocañas, L., & Camacho‐Morales, A. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.03.009 · Cited by 32
“In this regard, several research groups have reported that MIA during pregnancy sets neuronal defects leading to behavioral anomalies in the offspring, such as epilepsy, schizophrenia (SZ), cerebral palsy, Parkinson disease (PD), Alzheimer disease (AD) and also ASD (Estes and McAllister, 2016; Knuesel et al., 2014).”
Lenz, K. M., Pickett, L. A., Wright, C. L., Galan, A., & McCarthy, M. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-41258-2 · Cited by 30
Yasumatsu, K., Nagao, J.-I., Arita-Morioka, K.-I., Narita, Y., Tasaki, S., Toyoda, K., Ito, S., Kido, H., & Tanaka, Y. (2020) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.19-0156 · Cited by 28
“Several epidemiological reports indicate that one of the risk factors to induce mia is a maternal infection with pathogens [2, 7, 29]. to investigate the relationships between mia and ASD-like behaviors of offspring, animal models of MIA induced by polyinosinic:polycytidylic acid (poly(i:C)) to…”
Patel, S., Cooper, M. N., Jones, H. F., Whitehouse, A., Dale, R. C., & Guastella, A. J. (2020) · Psychological Medicine · doi:10.1017/s0033291720001580 · Cited by 32
“…animal models have led to proposals that MIA may increase fetal risk for the development of neuropsychiatric and neurodevelopmental disorders later in life, such as autism spectrum disorder (ASD), schizophrenia, mood disorders, and anxiety disorders (Estes & McAllister, 2016; Knuesel et al., 2014).”
BackgroundCOVID-19 in babies: Knowledge for neonatal care
Green, J., Petty, J., Bromley, P., Walker, K., & Jones, L. (2020) · Journal of Neonatal Nursing · doi:10.1016/j.jnn.2020.06.005 · Cited by 32
Benson, C. A., Powell, H. R., Liput, M., Dinham, S., Freedman, D. A., Ignatowski, T. A., Stachowiak, E. K., & Stachowiak, M. K. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00233 · Cited by 32
COVID-19 and Pregnancy: Vertical Transmission and Inflammation Impact on Newborns
Joma, M., Fovet, C.-M., Seddiki, N., Gressèns, P., & Laforge, M. (2021) · Vaccines · doi:10.3390/vaccines9040391 · Cited by 32
“Maternal immune activation (MIA) appears to act as a neurodevelopmental disease increasing the risk of neuronal epigenetic modification resulting in neuronal disorders later in life [98].”
BackgroundTallarek, A., Urbschat, C., Brito, L. F., Stanelle‐Bertram, S., Krasemann, S., Frascaroli, G., Thiele, K., Wieczorek, A., Felber, N., Lütgehetmann, M., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.698578 · Cited by 31
Viruses and autism: A Bi-mutual cause and effect
Al‐Beltagi, M., Saeed, N. K., Elbeltagi, R. M., Bediwy, A. S., Aftab, S. A. S., & Alhawamdeh, R. (2023) · World Journal of Virology · doi:10.5501/wjv.v12.i3.172 · Cited by 32
Zuiki, M., Chiyonobu, T., Yoshida, M., Maeda, H., Yamashita, S., Kidowaki, S., Hasegawa, T., Gotoh, H., Nomura, T., Ono, K., et al. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.06.004 · Cited by 30
Conceptual and methodological flaws undermine claims of a link between the gut microbiome and autism
Mitchell, K. J., Dahly, D. L., & Bishop, D. (2025) · Neuron · doi:10.1016/j.neuron.2025.10.006 · Cited by 35
Immunoglobulin-Like Receptors and Their Impact on Wiring of Brain Synapses
Cameron, S., & McAllister, A. K. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-120417-031513 · Cited by 28
Self-citationNazzari, S., & Frigerio, A. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.10.010 · Cited by 29
Maternal Interleukin-6 Is Associated With Macaque Offspring Amygdala Development and Behavior
Ramirez, J. S. B., Graham, A. M., Thompson, J. R., Zhu, J. Y., Sturgeon, D., Bagley, J. L., Thomas, E., Papadakis, S., Bah, M., Perrone, A. J., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz188 · Cited by 29
Pregnant people deserve the protection offered by SARS-CoV-2 vaccines
Maykin, M. M., Heuser, C. C., & Feltovich, H. M. (2020) · Vaccine · doi:10.1016/j.vaccine.2020.12.007 · Cited by 29
“Another concern is that placental injury may increase the risk of long-term adverse neurodevelopmental and other outcomes for affected infants, as it does for many conditions that affect the placenta [9].”
BackgroundTochitani, S. (2020) · Neuroscience Research · doi:10.1016/j.neures.2020.11.006 · Cited by 30
“The maternal immune activation (MIA) model is a rodent model that mimics infection during pregnancy (Estes and McAllister, 2016; Kentner et al., 2019).”
Theoharides, T. C. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11090860 · Cited by 29
Developmental Stressors Induce Innate Immune Memory in Microglia and Contribute to Disease Risk
Carloni, E., Ramos, A., & Hayes, L. N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222313035 · Cited by 30
Varied Composition and Underlying Mechanisms of Gut Microbiome in Neuroinflammation
Farooq, R. K., Alamoudi, W., Alhibshi, A., Rehman, S., Sharma, A. R., & Abdulla, F. A. (2022) · Microorganisms · doi:10.3390/microorganisms10040705 · Cited by 31
Fessel, J. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01879-0 · Cited by 28
“Because they confirm that events as long ago as in-utero or infancy, may influence subsequent SCZ, a brief mention is made here about the several prospective studies following birth cohorts that are consistent with an association between viral or bacterial maternal infection and psychiatric disorders in offspring [37]…”
ResultInfluentialNeurodevelopmental toxicity induced by airborne particulate matter
Shang, M., Tang, M. X., & Xue, Y. (2022) · Journal of Applied Toxicology · doi:10.1002/jat.4382 · Cited by 30
“Microglia are innate immune cells in the brain that play a role in regu- lation of neuroinflammation and are associated with a variety of brain diseases (Estes & McAllister, 2016).”
BackgroundGuma, E., Cupo, L., Ma, W., Gallino, D., Moquin, L., Gratton, A. P., Devenyi, G. A., & Chakravarty, M. M. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2022.110642 · Cited by 32
Immune activation state modulates infant engram expression across development
Power, S. D., Stewart, E., Zielke, L. G., Byrne, E. P., Douglas, A., Luis, C. O. S., Lynch, L., & Ryan, T. J. (2023) · Science Advances · doi:10.1126/sciadv.adg9921 · Cited by 29
Stanelle‐Bertram, S., Gnirß, K., Speiseder, T., Thiele, S., Asante, I. A., Dreier, C., Kouassi, N. M., Preuß, A., Pilnitz-Stolze, G., Müller, U., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0236-1 · Cited by 29
Strzelewicz, A. R., Sanchez, E. O., Rondón-Ortiz, A. N., Raneri, A., Famularo, S. T., Bangasser, D. A., & Kentner, A. C. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.01.003 · Cited by 29
Aria, F., Bonini, S. A., Cattaneo, V., Premoli, M., Mastinu, A., Maccarinelli, G., & Memo, M. (2020) · Brain Sciences · doi:10.3390/brainsci10090620 · Cited by 28
Nakahara, K., Michikawa, T., Morokuma, S., Ogawa, M., Kato, K., Sanefuji, M., Shibata, E., Tsuji, M., Shimono, M., Kawamoto, T., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-91271-7 · Cited by 29
Alteration of NMDA receptor trafficking as a cellular hallmark of psychosis
Espana, A., Seth, H., Jézéquel, J., Huang, T., Bouchet, D., Lepleux, M., Gréa, H., Bechter, K., Schneider, M., Hanse, E., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01549-7 · Cited by 29
“, kynurenic acid is a NMDAR antagonist) [33].”
BackgroundResultZou, W., Liu, J., Jiao, Y., Sun, Y., Chen, N., Zhou, L., Guan, X., Wang, J., Wei, W., Han, C., et al. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.339002 · Cited by 30
“Discussion Prenatal MIA caused by infection during pregnancy can cause acute and chronic changes in the structure and function of the fetal central nervous system (Estes and McAllister, 2016).”
BackgroundCouch, A. C. M., Solomon, S., Duarte, R. R. R., Marrocu, A., Sun, Y., Sichlinger, L., Matulevičiūtė, R., Polit, L. D., Hanger, B., Brown, A. M., et al. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.02.007 · Cited by 28
Martín-González, N. S., Castro-Quintas, Á., Marqués-Feixa, L., Ayesa‐Arriola, R., López, M., & Fañanás, L. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105178 · Cited by 27
Emmerich, K., White, D. T., Kambhampati, S. P., Casado, G. L., Tian-ming Fu, B., Chunawala, Z., Sahoo, A., Nimmagadda, S., Krishnan, N., Saxena, M. T., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04898-9 · Cited by 28
Dysregulated immunity in SARS-CoV-2 infected pregnant womenPreprint
Sherer, M. L., Lei, J., Creisher, P. S., Jang, M., Reddy, R., Voegtline, K., Olson, S., Littlefield, K. E., Park, H.-S., Ursin, R. L., et al. (2020) · medRxiv · doi:10.1101/2020.11.13.20231373 · Cited by 28
Update on the neurodevelopmental theory of depression: is there any 'unconscious code'?
Gałecka, M., Bliźniewska-Kowalska, K., Maes, M., Su, K.-P., & Gałecki, P. (2021) · Pharmacological Reports · doi:10.1007/s43440-020-00202-2 · Cited by 27
“Animal studies confirm that the later disturbances in utero occur due to maternal immune activation (MIA), the less important this is for the brain of the developing fetus [30].”
BackgroundGillespie, B., Panthi, S., Sundram, S., & Hill, R. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105488 · Cited by 32
“…for neurodevelopmental disorders in unborn children exposed to maternal infection, it is thought that the mechanism by which infection increases risk is driven by activation of the maternal immune system (Smith et al., 2007; Estes and McAllister, 2016b; Brown and Meyer, 2018; Solek et al., 2018).”
Cantando, I., Centofanti, C., D’Alessandro, G., Limatola, C., & Bezzi, P. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1354259 · Cited by 27
Li, Y., Dugyala, S., Ptacek, T., Gilmore, J. H., & Frӧhlich, F. (2018) · eNeuro · doi:10.1523/eneuro.0313-18.2018 · Cited by 27
“Epidemiological data of neurodevelopmental disorders motivates MIA studies in animal models (Meyer and Feldon, 2010; Estes and McAllister, 2016).”
BackgroundMethodInfluentialChaney, C., López, M., Wiley, K. S., Meyer, C., & Valeggia, C. R. (2019) · Journal of Racial and Ethnic Health Disparities · doi:10.1007/s40615-019-00622-8 · Cited by 27
Li, Z., Li, Y., & Jiao, J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913978116 · Cited by 26
Inflammatory modulation of the associations between prenatal maternal depression and neonatal brain
Wu, Y., Zhang, H., Wang, C., Broekman, B. F. P., Chong, Y. S., Shek, L. P., Gluckman, P. D., Meaney, M. J., Fortier, M. V., & Qiu, A. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0774-0 · Cited by 27
“Based on above, we hypothesized that inflammatory cytokines may be critical moderators in altering the fetal brain development upon the maternal environment, particularly in the brain regions related to affective psychopathology, such as the amygdala, hippocampus, frontal and sensory cortex [15, 16].”
BackgroundInflammation as a Mechanism of Bipolar Disorder Neuroprogression
Barichello, T., Giridharan, V. V., Bhatti, G. S., Sayana, P., Doifode, T., Macêdo, D. S., & Quevedo, J. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_173 · Cited by 28
General health and mortality in Tourette syndrome and chronic tic disorder: A mini-review
de la Cruz, L. F., & Mataix‐Cols, D. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.005 · Cited by 31
“Given the increased attention to maternal immune activation in neuropsychiatric disorders (Estes and McAllister, 2016; Knuesel et al., 2014), future studies could examine whether”
Association of Maternal Immune Activation during Pregnancy and Neurologic Outcomes in Offspring
Jain, S., Baer, R. J., McCulloch, C. E., Rogers, E. E., Rand, L., Jelliffe‐Pawlowski, L. L., & Piao, X. (2021) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2021.04.069 · Cited by 28
Yu, X., Rahman, M. M., Wang, Z., Carter, S., Schwartz, J. D., Chen, Z., Eckel, S. P., Hackman, D. A., Chen, J., Xiang, A. H., et al. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112590 · Cited by 29
Zhao, T., Wu, D., Du, J., Liu, G., Ji, G., Wang, Z., Peng, F., Man, L., Zhou, W., & Hao, A. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.818423 · Cited by 28
“Previous studies have shown that FA may affect NF-κB and MAPK signaling-dependent events in BV2 cells (Feng et al., 2011).”
BackgroundNaudé, P. J. W., Pariante, C. M., Hoffman, N., Koopowitz, S., Donald, K. A., Zar, H. J., & Stein, D. J. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.07.001 · Cited by 26
“…necrosis factor-alpha (TNF-α), can interfere with neurobiological processes in critical windows of brain development (Deverman and Patterson, 2009; Morimoto and Nakajima, 2019), which can lead to cognitive and behavioural impairments in offspring (Estes and McAllister, 2016; Knuesel et al., 2014).”
BackgroundImmune Responses to SARS-CoV-2 in Pregnancy: Implications for the Health of the Next Generation
Shook, L. L., Fourman, L. T., & Edlow, A. G. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2200414 · Cited by 27
Schizophrenia as metabolic disease. What are the causes?
Helaly, A. M., & Ghorab, D. S. (2023) · Metabolic Brain Disease · doi:10.1007/s11011-022-01147-6 · Cited by 27
“The evidence of this hypothesis is based on experimental animal work supported by clinical statistical data (Estes and McAllister 2016).”
BackgroundThe impact of maternal immune activation on embryonic brain development
McEwan, F., Glazier, J. D., & Hager, R. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1146710 · Cited by 30
“This is evidenced following genetic studies, which show that a high proportion of genes linked to NDDs are implicated in cellular proliferation and differentiation (Ernst, 2016).”
BackgroundInfluentialGreene, R. K., Walsh, E. C., Mosner, M. G., & Dichter, G. S. (2018) · Biological Psychology · doi:10.1016/j.biopsycho.2018.12.008 · Cited by 29
“…during pregnancy has shown deleterious effects, and hospital admissions due to maternal viral infection in the fi rst trimester or bacterial infection within the second trimester signi fi cantly increased the risk of o ff spring developing ASD (Atladóttir et al., 2010; Estes & McAllister, 2016).”
BackgroundVigli, D., Palombelli, G., Fanelli, S., Calamandrei, G., Canese, R., Mosca, L., Scattoni, M. L., & Ricceri, L. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.05.009 · Cited by 28
The contributions of parental lactation on offspring development: It's not udder nonsense!
Wijenayake, S., Martz, J., Lapp, H. E., Storm, J. A., Champagne, F. A., & Kentner, A. C. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105375 · Cited by 31
“Infection during pregnancy is also associated with an increased risk for the offspring to develop neurodevelopmental disorders in later life, including autism and schizophrenia (Estes and McAllister, 2016; Han et al., 2021).”
BackgroundMicrobiome and Pregnancy Dysbiosis: A Narrative Review on Offspring Health
Biagioli, V., Matera, M., Ramenghi, L. A., Falsaperla, R., & Striano, P. (2025) · Nutrients · doi:10.3390/nu17061033 · Cited by 30
“…such as chronic inflammatory bowel disease (IBD), autoimmune diseases, asthma [41], and low-grade systemic inflammation, like excess weight and obesity [42], gestational diabetes [43], and periodontal disease [44], as well as exposure to stress and polluting and toxic environmental factors [45].”
UBE3A regulates the transcription of IRF, an antiviral immunity
Furumai, R., Tamada, K., Liu, X., & Takumi, T. (2019) · Human Molecular Genetics · doi:10.1093/hmg/ddz019 · Cited by 26
“A number of other studies have shown that cytokine levels in the blood, brain and cerebrospinal fluid of autistic subjects are elevated compared to those of healthy individuals (81,82).”
ResultThe Synaptic Dysregulation in Adolescent Rats Exposed to Maternal Immune Activation
Cieślik, M., Gąssowska-Dobrowolska, M., Zawadzka, A., Frontczak‐Baniewicz, M., Gewartowska, M., Dominiak, A., Czapski, G. A., & Adamczyk, A. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.555290 · Cited by 25
Prenatal Programming of Neurodevelopment: Structural and Functional Changes
Demers, C. H., Aran, Ö., Glynn, L. M., & Davis, E. P. (2021) · Springer eBooks · doi:10.1007/978-3-030-60159-1_9 · Cited by 25
Sullivan, G., Galdi, P., Borbye‐Lorenzen, N., Stoye, D. Q., Lamb, G. J., Evans, M. J., Skogstrand, K., Chandran, S., & Boardman, J. P. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.722489 · Cited by 26
“Given that HCA is associated with cerebral palsy among children born at term (68), and maternal immune activation in term pregnancies is linked to neurodevelopmental and psychiatric diagnoses (69), further work is warranted to determine the relevance of our observations in preterm infants to births at term complicated…”
BackgroundA Unifying Theory for Autism: The Pathogenetic Triad as a Theoretical Framework
Sarovic, D. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.767075 · Cited by 30
“Supporting this is that both mechanisms may result in cognitive dysfunction (203, 264, 265), and have been identified in other neuropsychiatric disorders (266).”
BackgroundKwon, J., Suessmilch, M., McColl, A., Cavanagh, J., & MORRIS, B. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-03216-9 · Cited by 26
“Conclusions The use of poly I:C administration to pregnant rats or mice, as a means of modelling the increased risk for schizophrenia caused by in utero exposure to infection, has become widespread (Zuckerman et al., 2003; Meyer et al., 2005; Estes and McAllister, 2016).”
BackgroundInfluentialThe marmoset as a model for investigating the neural basis of social cognition in health and disease
Samandra, R., Haque, Z. Z., Rosa, M. G. P., & Mansouri, F. A. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104692 · Cited by 23
Woolfenden, S. R., Farrar, M. A., Eapen, V., Masi, A., Wakefield, C. E., Badawi, N. A., Novak, I., Nassar, N., Lingam, R., & Dale, R. C. (2022) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.15289 · Cited by 28
Tao, Q., Shen, Y., Li, Y., Luo, H., Yuan, M., & Gan, J. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.1045865 · Cited by 26
Schwabenland, M., Mossad, O., Sievert, A., Peres, A. G., Ringel, E., Baasch, S., Kolter, J., Cascone, G., Dokalis, N., Vlachos, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38373-0 · Cited by 26
Metadata
- Authors
- Estes, M. L., & McAllister, A. K.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- McAllister, A. Kimberley
- Venue
- Science
- Published
- 2016-08-19
- Volume
- 353
- Issue
- 6301
- Pages
- 772-777
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC5650490
- OpenAlex
- W2515897135
- Semantic Scholar
- 70e346df06748a0e6435133309a1011e2a43f998
- Cited by
- 1,206
- References
- 86
- Citations by year
- 2026: 109 · 2025: 134 · 2024: 134 · 2023: 128 · 2022: 158 · 2021: 139 · 2020: 119 · 2019: 114 · 2018: 104 · 2017: 54 · 2016: 10
- FWCI
- 5.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01-NS060125-05)
- National Institute of Mental Health (P50-MH106438-01)
- Simons Foundation (321998)
- University of California Davis Research Investments in Science and Engineering Program
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal immune activation, maternal infection, autism spectrum disorder, schizophrenia, neuropsychiatric disorders, animal models, neuropathology, neuroimmunological diseases, molecular mechanisms, risk factors
- MeSH terms
- Autism Spectrum Disorder, Adolescent, Animals, Brain, Child, Child, Preschool, Disease Models, Animal, Female, Humans, Immune System, Immune System Diseases, Mothers, Pregnancy, Pregnancy Complications, Infectious, Risk Factors, Schizophrenia, Gastrointestinal Tract, Young Adult
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
