Cited by 282Tryptophan and brain disordersMaternal Mental Health During Pregnancy and PostpartumNeonatal and fetal brain pathology

The DOI matches its Crossref record; 156 of the 158 references it cites were found in a registry or an index.

Maternal Systemic Interleukin-6 During Pregnancy Is Associated With Newborn Amygdala Phenotypes and Subsequent Behavior at 2 Years of Age

Open access

Graham, Alice M., Rasmussen, Jerod M., Rudolph, Marc D., Heim, Christine M., Gilmore, John H., Styner, Martin, Potkin, Steven G., Entringer, Sonja, Wadhwa, Pathik D., Fair, Damien A., Buss, Claudia·2018·Biological Psychiatry

DOI 10.1016/j.biopsych.2017.05.027PMC PMC5723539

Open this paper in CoChat — free account

Abstract

Background Maternal inflammation during pregnancy increases the risk for offspring psychiatric disorders and other adverse long-term health outcomes. The influence of inflammation on the developing fetal brain is hypothesized as one potential mechanism but has not been examined in humans.Methods Participants were adult women (N = 86) who were recruited during early pregnancy and whose offspring were born after 34 weeks' gestation. A biological indicator of maternal inflammation (interleukin-6) that has been shown to influence fetal brain development in animal models was quantified serially in early, mid-, and late pregnancy. Structural and functional brain magnetic resonance imaging scans were acquired in neonates shortly after birth. Infants' amygdalae were individually segmented for measures of volume and as seeds for resting state functional connectivity. At 24 months of age, children completed a snack delay task to assess impulse control.Results Higher average maternal interleukin-6 concentration during pregnancy was prospectively associated with larger right amygdala volume and stronger bilateral amygdala connectivity to brain regions involved in sensory processing and integration (fusiform, somatosensory cortex, and thalamus), salience detection (anterior insula), and learning and memory (caudate and parahippocampal gyrus). Larger newborn right amygdala volume and stronger left amygdala connectivity were in turn associated with lower impulse control at 24 months of age, and mediated the association between higher maternal interleukin-6 concentrations and lower impulse control.Conclusions These findings provide new evidence in humans linking maternal inflammation during pregnancy with newborn brain and emerging behavioral phenotypes relevant for psychiatric disorders. A better understanding of intrauterine conditions that influence offspring disease susceptibility is warranted to inform targeted early intervention and prevention efforts.

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

Crossref · 10.1016/j.biopsych.2017.05.027

Cites

156 of 156 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

1 retracted

Subtyping Attention-Deficit/Hyperactivity Disorder Using Temperament Dimensions: Toward Biologically Based Nosologic Criteria
Karalunas, S. L., Fair, D., Musser, E. D., Aykes, K., Iyer, S. P., & Nigg, J. T. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2014.763 · Cited by 340
Self-citation
Retracted
Untitled work
(1978) · Medical Entomology and Zoology · Cited by 12,570
User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability.
Yushkevich, P. A., Piven, J., Hazlett, H. C., Smith, R. G., Ho, S., Gee, J. C., & Gerig, G. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.01.015 · Cited by 8,868
Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.018 · Cited by 7,429
Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging
Fox, M. D., & Raichle, M. E. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2201 · Cited by 6,700
A gradient of childhood self-control predicts health, wealth, and public safety
Moffitt, T. E., Arseneault, L., Belsky, D., Dickson, N., Hancox, R. J., Harrington, H., Houts, R., Poulton, R., Roberts, B. W., Ross, S., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010076108 · Cited by 4,885
Principles of interleukin (IL)-6-type cytokine signalling and its regulation
HEINRICH, P. C., BEHRMANN, I., HAAN, S., HERMANNS, H. M., MÜLLER-NEWEN, G., & SCHAPER, F. (2003) · Biochemical Journal · doi:10.1042/bj20030407 · Cited by 3,272
Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold
Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910330508 · Cited by 3,202
The amygdala: vigilance and emotion
Davis, M., & Whalen, P. J. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000812 · Cited by 2,882
Unbiased average age-appropriate atlases for pediatric studies
Fonov, V., Evans, A. C., Botteron, K., Almli, C. R., McKinstry, R. C., & Collins, D. L. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.033 · Cited by 2,290

Show all 158 references

Sorted by citations

Maternal immune activation and neuroinflammation in human neurodevelopmental disorders
Han, V. X., Patel, S., Jones, H. F., & Dale, R. C. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00530-8 · Cited by 683
Maternal IL-6 during pregnancy can be estimated from newborn brain connectivity and predicts future working memory in offspring
Rudolph, M. D., Graham, A. M., Feczko, E., Miranda-Dominguez, O., Rasmussen, J. M., Nardos, R., Entringer, S., Wadhwa, P. D., Buss, C., & Fair, D. A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0128-y · Cited by 374
Self-citation
Cytokine Research in Depression: Principles, Challenges, and Open Questions
Himmerich, H., Patsalos, O., Lichtblau, N., Ibrahim, M. A. A., & Dalton, B. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00030 · Cited by 313
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271
Inflammation: A Proposed Intermediary Between Maternal Stress and Offspring Neuropsychiatric Risk
Hantsoo, L., Kornfield, S., Anguera, M. C., & Epperson, C. N. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.08.018 · Cited by 269
Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes
Walsh, K., McCormack, C. A., Webster, R., Pinto, A., Lee, S., Feng, T., Krakovsky, H. S., O’Grady, S. M., Tycko, B., Champagne, F. A., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1905890116 · Cited by 273
Neurodevelopmental Resilience and Susceptibility to Maternal Immune Activation
Meyer, U. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.08.001 · Cited by 230
Association of prenatal maternal psychological distress with fetal brain growth, metabolism, and cortical maturation.
Wu, Y., Lu, Y.-C., Jacobs, M., Pradhan, S., Kapse, K., Zhao, L., Niforatos-Andescavage, N., Vezina, G., du Plessis, A. J., & Limperopoulos, C. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2019.19940 · Cited by 218
Maternal Interleukin-6 concentration during pregnancy is associated with variation in frontolimbic white matter and cognitive development in early life
Rasmussen, J. M., Graham, A. M., Entringer, S., Gilmore, J. H., Styner, M. A., Fair, D. A., Wadhwa, P. D., & Buß, C. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.04.020 · Cited by 215
Self-citation
Antenatal depression programs cortisol stress reactivity in offspring through increased maternal inflammation and cortisol in pregnancy: The Psychiatry Research and Motherhood – Depression (PRAM-D) Study
Osborne, S., Biaggi, A., Chua, T.-E., Preez, A. D., Hazelgrove, K. M., Nikkheslat, N., Previti, G., Zunszain, P. A., Conroy, S., & Pariante, C. M. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.06.017 · Cited by 221
Schizophrenia and influenza at the centenary of the 1918–1919 Spanish Influenza Pandemic: mechanisms of psychosis risk
Kępińska, A. P., Iyegbe, C. O., Vernon, A. C., Yolken, R., Murray, R. M., & Pollak, T. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00072 · Cited by 193
Maternal Cortisol Concentrations During Pregnancy and Sex-Specific Associations With Neonatal Amygdala Connectivity and Emerging Internalizing Behaviors
Graham, A. M., Rasmussen, J. M., Entringer, S., Ben Ward, E., Rudolph, M. D., Gilmore, J. H., Styner, M., Wadhwa, P. D., Fair, D. A., & Buss, C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.023 · Cited by 203
Self-citation
Perinatal Maternal Depressive Symptoms as an Issue for Population Health
Meaney, M. J. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2018.17091031 · Cited by 216
Maternal inflammation and its ramifications on fetal neurodevelopment
Kwon, H., Choi, G. B., & Huh, J. R. (2022) · Trends in Immunology · doi:10.1016/j.it.2022.01.007 · Cited by 204
Immune Dysregulation in Autism Spectrum Disorder: What Do We Know about It?
Robinson-Agramonte, M. D. L. A., Noris García, E., Fraga Guerra, J., Vega Hurtado, Y., Antonucci, N., Semprún-Hernández, N., Schultz, S., & Siniscalco, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063033 · Cited by 176
Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health
Heim, C. M., Entringer, S., & Buss, C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.011 · Cited by 158
Self-citation
Increasing Role of Maternal Immune Activation in Neurodevelopmental Disorders
Boulanger-Bertolus, J., Pancaro, C., & Mashour, G. A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00230 · Cited by 161
COVID-19 in pregnancy: implications for fetal brain development
Shook, L. L., Sullivan, E. L., Lo, J. O.-T., Perlis, R. H., & Edlow, A. G. (2022) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2022.02.004 · Cited by 146
Integrated analysis of environmental and genetic influences on cord blood DNA methylation in new-borns
Czamara, D., Eraslan, G., Page, C. M., Lahti, J., Lahti-Pulkkinen, M., Hämäläinen, E., Kajantie, E., Laivuori, H., Villa, P. M., Reynolds, R. M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10461-0 · Cited by 143
Self-citation
Association between persistent endocrine-disrupting chemicals (PBDEs, OH-PBDEs, PCBs, and PFASs) and biomarkers of inflammation and cellular aging during pregnancy and postpartum
Zota, A. R., Geller, R. J., Romano, L. E., Coleman‐Phox, K., Adler, N. E., Parry, E., Wang, M., Park, J.-S., Elmi, A. F., Laraia, B. A., et al. (2018) · Environment International · doi:10.1016/j.envint.2018.02.044 · Cited by 135
The Interplay Between Nutrition and Stress in Pregnancy: Implications for Fetal Programming of Brain Development
Lindsay, K. L., Buß, C., Wadhwa, P. D., & Entringer, S. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.021 · Cited by 148
Self-citation
Behavioral, neuroanatomical, and molecular correlates of resilience and susceptibility to maternal immune activation
Mueller, F. S., Scarborough, J., Schalbetter, S. M., Richetto, J., Kim, E., Couch, A. C. M., Yee, Y., Lerch, J. P., Vernon, A. C., Weber‐Stadlbauer, U., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00952-8 · Cited by 131
Prenatal Immune and Endocrine Modulators of Offspring's Brain Development and Cognitive Functions Later in Life
Schepanski, S. N., Buß, C., Hanganu‐Opatz, I. L., & Arck, P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02186 · Cited by 137
Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy
Wu, Y., De Asis-Cruz, J., & Limperopoulos, C. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02449-0 · Cited by 124
“The literature points to a relationship between maternal Interleukin-6 concentration during pregnancy and altered newborn brain structure and functional connectivity [140, 141].”
Background
The Impact of Infection in Pregnancy on Placental Vascular Development and Adverse Birth Outcomes
Weckman, A. M., Ngai, M., Wright, J. K., McDonald, C. R., & Kain, K. C. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01924 · Cited by 137
Early Social Adversity, Altered Brain Functional Connectivity, and Mental Health
Holz, N. E., Berhe, O., Sacu, S., Schwarz, E., Tesarz, J., Heim, C. C., & Tost, H. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.10.019 · Cited by 114
Self-citation
The role of maternal immune activation in altering the neurodevelopmental trajectories of offspring: A translational review of neuroimaging studies with implications for autism spectrum disorder and schizophrenia
Guma, E., Plitman, E., & Chakravarty, M. M. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.020 · Cited by 108
Intergenerational transmission of depression: clinical observations and molecular mechanisms
Sawyer, K. M., Zunszain, P. A., Dazzan, P., & Pariante, C. M. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0265-4 · Cited by 111
Maternal Immune Activation and Related Factors in the Risk of Offspring Psychiatric Disorders
Conway, F., & Brown, A. S. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00430 · Cited by 88
Prenatal stress causes intrauterine inflammation and serotonergic dysfunction, and long-term behavioral deficits through microbe- and CCL2-dependent mechanisms
Chen, H. J., Antonson, A. M., Rajasekera, T. A., Patterson, J. M., Bailey, M. T., & Gur, T. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00876-5 · Cited by 92
Persistently High Levels of Maternal Antenatal Inflammation Are Associated With and Mediate the Effect of Prenatal Environmental Adversities on Neurodevelopmental Delay in the Offspring
Girchenko, P. V., Lahti‐Pulkkinen, M., Heinonen, K., Reynolds, R. M., Laivuori, H. M., Lipsanen, J. O., Villa, P., Hämäläinen, E. K., Kajantie, E., Lahti, J. M. T., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.12.004 · Cited by 81
Maternal inflammation during pregnancy and offspring psychiatric symptoms in childhood: Timing and sex matter
Giollabhui, N. M., Breen, E. C., Murphy, S. K., Maxwell, S. D., Cohn, B. A., Krigbaum, N. Y., Cirillo, P. M., Perez, C. M., Alloy, L. B., Drabick, D. A. G., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.01.009 · Cited by 88
Beyond the HPA-axis: Exploring maternal prenatal influences on birth outcomes and stress reactivity
Nazzari, S., Fearon, P. R. M., Rice, F. J., Dottori, N., Ciceri, F., Molteni, M., & Frigerio, A. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.11.018 · Cited by 79
Newborn amygdala connectivity and early emerging fear
Thomas, E., Buß, C., Rasmussen, J. M., Entringer, S., Ramirez, J. S. B., Marr, M. C., Rudolph, M. D., Gilmore, J. H., Styner, M. A., Wadhwa, P. D., et al. (2018) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2018.12.002 · Cited by 77
Self-citation
Association of Prenatal Exposure to Early-Life Adversity With Neonatal Brain Volumes at Birth
Triplett, R. L., Lean, R. E., Parikh, A. N., Miller, J. P., Alexopoulos, D. K., Kaplan, S., Meyer, D., Adamson, C. L., Smyser, T. A., Rogers, C. E., et al. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.7045 · Cited by 73
Early or Late Gestational Exposure to Maternal Immune Activation Alters Neurodevelopmental Trajectories in Mice: An Integrated Neuroimaging, Behavioral, and Transcriptional Study
Guma, E., Bordignon, P. D. C., Devenyi, G. A., Gallino, D., Anastassiadis, C., Cvetkovska, V., Barry, A., Snook, E., Germann, J., Greenwood, C. M. T., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.03.017 · Cited by 73
Microbiota-immune-brain interactions: A lifespan perspective
Ratsika, A., Cruz-Pereira, J. S., Lynch, C. M. K., Clarke, G. A., & Cryan, J. F. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102652 · Cited by 83
Associations between different dimensions of prenatal distress, neonatal hippocampal connectivity, and infant memory
Scheinost, D., Spann, M. N., McDonough, L., Peterson, B. S., & Monk, C. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0677-0 · Cited by 73
Virus-Induced Maternal Immune Activation as an Environmental Factor in the Etiology of Autism and Schizophrenia
Massrali, A., Adhya, D., Srivastava, D. P., Baron‐Cohen, S., & Kotter, M. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.834058 · Cited by 83
Brain connectivity and socioeconomic status at birth and externalizing symptoms at age 2 years
Ramphal, B., Whalen, D. J., Kenley, J. K., Yu, Q., Smyser, C. D., Rogers, C. E., & Sylvester, C. M. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100811 · Cited by 70
Prenatal stress exposure and multimodal assessment of amygdala–medial prefrontal cortex connectivity in infants
Humphreys, K. L., Camacho, M. C., Roth, M. C., & Estes, E. C. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100877 · Cited by 67
Evaluation of maternal inflammation as a marker of future offspring ADHD symptoms: A prospective investigation
Gustafsson, H., Sullivan, E. L., Battison, E., Holton, K. F., Graham, A. M., Karalunas, S. L., Fair, D. A., Loftis, J. M., & Nigg, J. T. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.07.019 · Cited by 66
Self-citation
Translational opportunities in the prenatal immune environment: Promises and limitations of the maternal immune activation model
Bauman, M. D., & de Water, J. V. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104864 · Cited by 65
The Communication Between the Immune and Nervous Systems: The Role of IL-1β in Synaptopathies
Pozzi, D., Menna, E., Canzi, A., Desiato, G., Mantovani, C., & Matteoli, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00111 · Cited by 63
Prospective association of maternal psychosocial stress in pregnancy with newborn hippocampal volume and implications for infant social-emotional development
Moog, N. K., Nolvi, S., Kleih, T. S., Styner, M. A., Gilmore, J. H., Rasmussen, J. M., Heim, C. C., Entringer, S., Wadhwa, P. D., & Buß, C. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100368 · Cited by 66
Self-citation
Association between a Mixture of Per- and Polyfluoroalkyl Substances (PFAS) and Inflammatory Biomarkers in the Atlanta African American Maternal–Child Cohort
Tan, Y., Taibl, K. R., Dunlop, A. L., Barr, D. B., Panuwet, P., Yakimavets, V., Kannan, K., Corwin, E. J., Ryan, P. B., Eatman, J. A., et al. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c04688 · Cited by 58
Prenatal risk factors for internalizing and externalizing problems in childhood
Tien, J., Lewis, G. D., & Liu, J. (2019) · World Journal of Pediatrics · doi:10.1007/s12519-019-00319-2 · Cited by 59
Male fetus susceptibility to maternal inflammation: C-reactive protein and brain development
Hunter, S. K., Hoffman, M. C., D’Alessandro, A., Noonan, K., Wyrwa, A., Freedman, R., & Law, A. J. (2019) · Psychological Medicine · doi:10.1017/s0033291719003313 · Cited by 57
Screening for Anxiety in Adolescent and Adult Women: A Recommendation From the Women's Preventive Services Initiative
Gregory, K. D., Chelmow, D. P., Nelson, H. D., Niel, M. S. V., Conry, J. A., García, F., Kendig, S. M., O’Reilly, N., Qaseem, A., Ramos, D., et al. (2020) · Annals of Internal Medicine · doi:10.7326/m20-0580 · Cited by 55
Prenatal exposures and infant brain: Review of magnetic resonance imaging studies and a population description analysis
Pulli, E. P., Kumpulainen, V., Kasurinen, J. H., Korja, R., Merisaari, H., Karlsson, L., Parkkola, R. K., Saunavaara, J. P., Lähdesmäki, T., Scheinin, N. M., et al. (2018) · Human Brain Mapping · doi:10.1002/hbm.24480 · Cited by 56
Adverse Prenatal Exposures and Fetal Brain Development: Insights From Advanced Fetal Magnetic Resonance Imaging
Asis‐Cruz, J. D., Andescavage, N. N., & Limperopoulos, C. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.11.009 · Cited by 53
Human amygdala functional network development: A cross-sectional study from 3 months to 5 years of age
Gabard-Durnam, L. J., O’Muircheartaigh, J., Dirks, H., Dean, D., Tottenham, N., & Deoni, S. (2018) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2018.06.004 · Cited by 54
The Effects of Prenatal Exposure to Neighborhood Crime on Neonatal Functional Connectivity
Brady, R. G., Rogers, C. E., Prochaska, T., Kaplan, S., Lean, R. E., Smyser, T. A., Shimony, J. S., Slavich, G. M., Warner, B. B., Barch, D. M., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.01.020 · Cited by 50
Prenatal pregnancy-related anxiety predicts boys’ ADHD symptoms via placental C-reactive protein
Shao, S., Wang, J., Huang, K., Wang, S., Liu, H., Wan, S., Yan, S., Hao, J., Zhu, P., & Tao, F. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104797 · Cited by 50
Effects of Maternal Psychological Stress During Pregnancy on Offspring Brain Development: Considering the Role of Inflammation and Potential for Preventive Intervention
Graham, A. M., Doyle, O. J., Tilden, E. L., Sullivan, E. L., Gustafsson, H., Marr, M. C., Allen, M. C., & Seghete, K. L. M. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.10.012 · Cited by 56
Self-citation
The Implication of Mechanistic Approaches and the Role of the Microbiome in Polycystic Ovary Syndrome (PCOS): A Review
Mukherjee, A. G., Wanjari, U. R., Kannampuzha, S., Murali, R., Namachivayam, A., Ganesan, R., Dey, A., Babu, A., Renu, K., Vellingiri, B., et al. (2023) · Metabolites · doi:10.3390/metabo13010129 · Cited by 56
Newborn amygdalar volumes are associated with maternal prenatal psychological distress in a sex-dependent way
Lehtola, S. J., Tuulari, J. J., Scheinin, N. M., Karlsson, L., Parkkola, R., Merisaari, H., Lewis, J. D., Fonov, V. S., Louis Collins, D., Evans, A., et al. (2020) · NeuroImage: Clinical · doi:10.1016/j.nicl.2020.102380 · Cited by 51
Resting state functional MRI in infants with prenatal opioid exposure—a pilot study
Radhakrishnan, R., Elsaid, N., Sadhasivam, S., Reher, T. A., Hines, A. C., Yoder, K. K., Saykin, A. J., & Wu, Y. (2020) · Neuroradiology · doi:10.1007/s00234-020-02552-3 · Cited by 48
Effect of advanced parental age on pregnancy outcome and offspring health
Zhang, C., Yan, L., & Qiao, J. (2022) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-022-02533-w · Cited by 53
Understanding Vulnerability and Adaptation in Early Brain Development using Network Neuroscience
Graham, A. M., Marr, M. C., Buß, C., Sullivan, E. L., & Fair, D. A. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.01.008 · Cited by 50
Self-citation
Pathways linking childhood abuse history and current socioeconomic status to inflammation during pregnancy
Finy, M. S., & Christian, L. M. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.09.012 · Cited by 48
Placental dysfunction: The core mechanism for poor neurodevelopmental outcomes in the offspring of preeclampsia pregnancies
Liu, D., Gao, Q., Wang, Y., & Xiong, T. (2022) · Placenta · doi:10.1016/j.placenta.2022.07.014 · Cited by 48
White Matter Tract Changes Associated with Clinical Improvement in an Open-Label Trial Assessing Autologous Umbilical Cord Blood for Treatment of Young Children with Autism
Carpenter, K. L. H., Major, S. T., Tallman, C. W., Chen, L. W., Franz, L., Sun, J. M., Kurtzberg, J., Song, A. W., & Dawson, G. (2019) · Stem Cells Translational Medicine · doi:10.1002/sctm.18-0251 · Cited by 47
Interleukin (IL)-6: A Friend or Foe of Pregnancy and Parturition? Evidence From Functional Studies in Fetal Membrane Cells
Omere, C. I., Richardson, L., Saade, G. R., Bonney, E. A., Kechichian, T. B., & Menon, R. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00891 · Cited by 45
Immune regulation of neurodevelopment at the mother–foetus interface: the case of autism
Sotgiu, S., Manca, S., Gagliano, A., Minutolo, A., Melis, M. C., Pisuttu, G., Scoppola, C., Bolognesi, E., Clerici, M., Guerini, F. R., et al. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1211 · Cited by 46
In-depth characterization of congenital Zika syndrome in immunocompetent mice: Antibody-dependent enhancement and an antiviral peptide therapy
Camargos, V. N., Foureaux, G., Medeiros, D. D. C., da Silveira, V. T., Queiroz‐Junior, C. M., Matosinhos, A. L. B., Figueiredo, A. F. A., de Sousa, C. D. F., Moreira, T. P., Queiroz, V. F., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.05.014 · Cited by 43
Maternal immune activation primes deficiencies in adult hippocampal neurogenesis
Couch, A. C. M., Berger, T., Hanger, B., Matulevičiūtė, R., Srivastava, D. P., Thuret, S., & Vernon, A. C. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.07.021 · Cited by 44
How prenatal exposures shape the infant brain: Insights from infant neuroimaging studies
Dufford, A. J., Spann, M. N., & Scheinost, D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.017 · Cited by 45
Differential effects of early or late exposure to prenatal maternal immune activation on mouse embryonic neurodevelopment
Guma, E., Bordeleau, M., Ibáñez, F. G., Picard, K., Snook, E., Desrosiers-Grégoire, G., Spring, S., Lerch, J. P., Nieman, B. J., Devenyi, G. A., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114545119 · Cited by 42
Offspring born to influenza A virus infected pregnant mice have increased susceptibility to viral and bacterial infections in early life
Jacobsen, H., Gnirß, K., Tekin-Bubenheim, N., Kouassi, N. M., Batalla, I. B., Berenbrok, N., Wolff, M., dos Reis, V. P., Zickler, M., Scholl, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25220-3 · Cited by 43
Transmission of the adverse consequences of childhood maltreatment across generations: Focus on gestational biology
Moog, N. K., Heim, C. C., Entringer, S., Simhan, H. N., Wadhwa, P. D., & Buß, C. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173372 · Cited by 49
Self-citation
Preliminary evidence of increased striatal dopamine in a nonhuman primate model of maternal immune activation
Bauman, M. D., Lesh, T. A., Rowland, D. J., Schumann, C. M., Smucny, J., Kukis, D. L., Cherry, S. R., McAllister, A. K., & Carter, C. S. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0449-y · Cited by 43
Associations between Amygdala-Prefrontal Functional Connectivity and Age Depend on Neighborhood Socioeconomic Status
Ramphal, B., DeSerisy, M., Pagliaccio, D., Raffanello, E., Rauh, V., Tau, G. Z., Posner, J. E., Marsh, R., & Margolis, A. E. (2020) · Cerebral Cortex Communications · doi:10.1093/texcom/tgaa033 · Cited by 47
Maternal Perinatal Stress Trajectories and Negative Affect and Amygdala Development in Offspring
Marr, M. C., Graham, A. M., Feczko, E., Nolvi, S., Thomas, E., Sturgeon, D., Schifsky, E., Rasmussen, J. M., Gilmore, J. H., Styner, M. A., et al. (2023) · American Journal of Psychiatry · doi:10.1176/appi.ajp.21111176 · Cited by 46
Self-citation
Effects of Antipsychotic Drugs: Cross Talk Between the Nervous and Innate Immune System
Dinesh, A. A., Islam, J., Khan, J., Turkheimer, F., & Vernon, A. C. (2020) · CNS Drugs · doi:10.1007/s40263-020-00765-x · Cited by 40
Neuroendocrine and immune markers of maternal stress during pregnancy and infant cognitive development
Nazzari, S., Fearon, P. R. M., Rice, F. J., Ciceri, F., Molteni, M., & Frigerio, A. (2020) · Developmental Psychobiology · doi:10.1002/dev.21967 · Cited by 39
Exposure to prenatal maternal distress and infant white matter neurodevelopment
Demers, C. H., Bagonis, M., Al‐Ali, K., Garcia, S. E., Styner, M. A., Gilmore, J. H., Hoffman, M. C., Hankin, B. L., & Davis, E. P. (2021) · Development and Psychopathology · doi:10.1017/s0954579421000742 · Cited by 38
Self-citation
Maternal oxidative stress during pregnancy and offspring neurodevelopment
Buß, C. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.01.007 · Cited by 35
Neonatal White Matter Maturation Is Associated With Infant Language Development
Sket, G., Overfeld, J., Styner, M. A., Gilmore, J. H., Entringer, S., Wadhwa, P. D., Rasmussen, J. M., & Buß, C. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00434 · Cited by 34
Self-citation
Inflammation and the Potential Implication of Macrophage-Microglia Polarization in Human ASD: An Overview
Lampiasi, N., Bonaventura, R., Deidda, I., Zito, F., & Russo, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032703 · Cited by 39
Partial Support for an Interaction Between a Polygenic Risk Score for Major Depressive Disorder and Prenatal Maternal Depressive Symptoms on Infant Right Amygdalar Volumes
Acosta, H., Kantojärvi, K., Hashempour, N., Pelto, J., Scheinin, N. M., Lehtola, S. J., Lewis, J. D., Fonov, V. S., Collins, D. L., Evans, A., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa158 · Cited by 34
A hierarchical model of early brain functional network development
Gao, W. (2025) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2025.04.001 · Cited by 39
Antineuroinflammatory therapy: potential treatment for autism spectrum disorder by inhibiting glial activation and restoring synaptic function
Li, Y., Zhang, X., & Li, Y. (2019) · CNS Spectrums · doi:10.1017/s1092852919001603 · Cited by 33
The biological underpinnings of perinatal depressive symptoms: A multi-systems approach.
Nazzari, S., Fearon, P. R. M., Rice, F. J., Ciceri, F., Molteni, M., & Frigerio, A. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.05.023 · Cited by 34
Placental inflammatory cytokines mRNA expression and preschool children’s cognitive performance: a birth cohort study in China
Zhou, 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
A perspective on pre‐eclampsia and neurodevelopmental outcomes in the offspring: Does maternal inflammation play a role?
Maher, G. M., McCarthy, F. P., McCarthy, C., Kenny, L. C., Kearney, P. M., Khashan, A. S., & O’Keeffe, G. W. (2018) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2018.10.004 · Cited by 32
Maternal depressive symptoms, neonatal white matter, and toddler social-emotional development
Lautarescu, A., Bonthrone, A. F., Pietsch, M., Batalle, D., Cordero-Grande, L., Tournier, J.-D., Christiaens, D., Hajnal, J. V., Chew, A., Falconer, S., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02073-y · Cited by 29
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
Prefrontal Cortex and Amygdala Subregion Morphology Are Associated With Obesity and Dietary Self-control in Children and Adolescents
Kim, M. S., LUO, S. H., Azad, A., Campbell, C. E., Felix, K., Cabeen, R. P., Belcher, B. R., Kim, R., Gonzalez, M. S., & Herting, M. M. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.563415 · Cited by 31
Distinct effects of interleukin-6 and interferon-γ on differentiating human cortical neurons
Kathuria, A., Lopez-Lengowski, K., Roffman, J. L., & Karmacharya, R. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.04.007 · Cited by 29
Impact of Maternal Immune Activation on Nonhuman Primate Prefrontal Cortex Development: Insights for Schizophrenia
Hanson, K. L., Grant, S. E., Funk, L. H., Schumann, C. M., & Bauman, M. D. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.04.004 · Cited by 34
Parsing ADHD With Temperament Traits
Nigg, J. T. (2022) · Current Directions in Psychological Science · doi:10.1177/09637214221098079 · Cited by 31
The programming role of maternal antenatal inflammation on infants’ early neurodevelopment: A review of human studies
Nazzari, 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
Self-citation
Neuroimaging in infants with prenatal opioid exposure: Current evidence, recent developments and targets for future research
Radhakrishnan, R., Grecco, G. G., Stolze, K., Atwood, B. K., Jennings, S. G., Lien, I. Z., Saykin, A. J., & Sadhasivam, S. (2020) · Journal of Neuroradiology · doi:10.1016/j.neurad.2020.09.009 · Cited by 31
Soil-transmitted helminth infection in pregnancy and long-term child neurocognitive and behavioral development: A prospective mother-child cohort in Benin
Garrison, A., Boivin, M. J., Khoshnood, B., Courtin, D., Alao, J. M., Mireku, M. O., Ibikounlé, M., Massougbodji, A., Cot, M., & Bodeau‐Livinec, F. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009260 · Cited by 34
Sex-Specific Cytokine Responses and Neurocognitive Outcome after Blood Transfusions in Preterm Infants
Benavides, A., Bell, E., Georgieff, M., Josephson, C., Stowell, S., Feldman, H., Nalbant, D., Tereshchenko, A., Sola-Visner, M., & Nopoulos, P. (2021) · Pediatric Research · doi:10.1038/s41390-021-01536-0 · Cited by 27
Exposure to childhood maltreatment and systemic inflammation across pregnancy: The moderating role of depressive symptomatology
Kleih, T. S., Entringer, S., Scholaske, L., Kathmann, N., de Punder, K., Heim, C. C., Wadhwa, P. D., & Buß, C. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.02.004 · Cited by 31
Self-citation
Maternal adverse childhood experiences and infant subcortical brain volume
Demers, C. H., Hankin, B. L., Hennessey, E. P., Haase, M. H., Bagonis, M. M., Kim, S. H., Gilmore, J. H., Hoffman, M. C., Styner, M. A., & Davis, E. P. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100487 · Cited by 29
Self-citation
Acute IL-6 exposure triggers canonical IL6Ra signaling in hiPSC microglia, but not neural progenitor cells
Couch, 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

Authors: Graham, A. M., Rasmussen, J. M., Rudolph, M. D., Heim, C. M., Gilmore, J. H., Styner, M., Potkin, S. G., Entringer, S., Wadhwa, P. D., Fair, D. A., & Buss, C.
Affiliations: Oregon Health & Science University (US)
University of California, Irvine (US)
University of North Carolina at Chapel Hill (US)
Corresponding author: Buss, Claudia
ORCID: Graham, Alice M.
Rasmussen, Jerod M.
Rudolph, Marc D.
Gilmore, John H.
Styner, Martin
Potkin, Steven G.
Entringer, Sonja
Wadhwa, Pathik D.
Fair, Damien A.
Buss, Claudia
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2018-01
Volume: 83
Issue: 2
Pages: 109-119
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2017.05.027
PMC: PMC5723539
OpenAlex: W2694505964
Cited by: 282
References: 158
Citations by year: 2026: 19 · 2025: 25 · 2024: 34 · 2023: 31 · 2022: 37 · 2021: 42 · 2020: 44 · 2019: 24 · 2018: 24
FWCI: 8.54
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (am, 340 d)
Locations: Biological Psychiatry (acceptedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: U.S. Public Health Service (R01 HD060628, R01 MH091351, UG3 OD-O23349, F32 MH105283, R00 MH091238, R01 MH096773)
Bill & Melinda Gates Foundation
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
Keywords: impulse control, prenatal inflammation, fetal brain development, mediation, early childhood behavior
MeSH terms: Adult, Amygdala, Child Behavior, Child, Preschool, Female, Humans, Impulsive Behavior, Infant, Newborn, Magnetic Resonance Imaging, Male, Nerve Net, Organ Size, Pregnancy, Prenatal Exposure Delayed Effects, Interleukin-6, Young Adult, Functional Neuroimaging

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

Maternal Systemic Interleukin-6 During Pregnancy Is Associated With Newborn Amygdala Phenotypes and Subsequent Behavior at 2 Years of Age

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks