The DOI matches its Crossref record; 240 of the 240 references it cites were found in a registry or an index.
The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders
Open accessAbstract
The developing immune system and central nervous system in the fetus and child are extremely sensitive to both exogenous and endogenous signals. Early immune system programming, leading to changes that can persist over the life course, has been suggested, and other evidence suggests that immune dysregulation in the early developing brain may play a role in neurodevelopmental disorders such as autism spectrum disorder and schizophrenia. The timing of immune dysregulation with respect to gestational age and neurologic development of the fetus may shape the elicited response. This creates a possible sensitive window of programming or vulnerability. This review will explore the effects of maternal prenatal and infant nutritional status (from conception until early childhood) as well as maternal prenatal stress and anxiety on early programming of immune function, and how this might influence neurodevelopment. We will describe fetal immune system development and maternal-fetal immune interactions to provide a better context for understanding the influence of nutrition and stress on the immune system. Finally, we will discuss the implications for prevention of neurodevelopmental disorders, with a focus on nutrition. Although certain micronutrient supplements have shown to both reduce the risk of neurodevelopmental disorders and enhance fetal immune development, we do not know whether their impact on immune development contributes to the preventive effect on neurodevelopmental disorders. Future studies are needed to elucidate this relationship, which may contribute to a better understanding of preventative mechanisms. Integrating studies of neurodevelopmental disorders and prenatal exposures with the simultaneous evaluation of neural and immune systems will shed light on mechanisms that underlie individual vulnerability or resilience to neurodevelopmental disorders and ultimately contribute to the development of primary preventions and early interventions.
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“This is in keeping with a large body of research showing that maternal physiology, particularly stress (85–87) and nutrition (88–90), can greatly impact the neural and behavioral development of offspring.”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [90]
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Items 201–240 of 240
Immunobiology of gestational zinc deficiency
Wellinghausen, N. (2001) · British Journal Of Nutrition · doi:10.1079/bjn2000298 · Cited by 76
Prenatal Stress and Risk of Asthma Hospitalization in the Offspring
Khashan, A. S., Wicks, S., Dalman, C., Henriksen, T. B., Li, J., Mortensen, P. B., & Kenny, L. C. (2012) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31825ac5e7 · Cited by 75
Effect of parity on fetal and maternal microchimerism: interaction of grafts within a host?
Gammill, H. S., Guthrie, K. A., Aydelotte, T. M., Waldorf, K. M. A., & Nelson, J. L. (2010) · Blood · doi:10.1182/blood-2010-02-270942 · Cited by 74
Prenatal Endocrine Activation Alters Postnatal Cellular Immunity in Infant Monkeys
Coe, C. L., Lubach, G. R., Karaszewski, J. W., & Ershler, W. B. (1996) · Brain Behavior and Immunity · doi:10.1006/brbi.1996.0020 · Cited by 68
Prenatal Stress and Risk of Infectious Diseases in Offspring
Nielsen, N. M., Hansen, A. V., Simonsen, J., & Hviid, A. P. (2011) · American Journal of Epidemiology · doi:10.1093/aje/kwq492 · Cited by 68
Protective effect of noninherited maternal HLA-DR antigens on rheumatoid arthritis development
Feitsma, A. L., Worthington, J., Mil, A. H. M. V. D. H., Plant, D., Thomson, W., Ursum, J., van Schaardenburg, D., van der Horst-Bruinsma, I. E., van Rood, J. J., Huizinga, T. W. J., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710260104 · Cited by 67
Oh, S.-Y., Zheng, T., Bailey, M. L., Barber, D. L., Schroeder, J. T., Kim, Y., & Zhu, Z. (2006) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2006.08.029 · Cited by 67
Maternal and fetal antibrain antibodies in development and disease
Fox, E., Amaral, D. G., & de Water, J. V. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22052 · Cited by 63
Effects of maternal breathing rate, psychiatric status, and cortisol on fetal heart rate
Monk, C. E., Fifer, W. P., Myers, M. M., Bagiella, E., Duong, J., Chen, I. S., Leotti, L. A., & Altincatal, A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20513 · Cited by 63
Patterson, P. H. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.09.008 · Cited by 62
Sternthal, M. J., Enlow, M. B., Cohen, S., Canner, M. J., STAUDENMAYER, J. W., Tsang, K., & Wright, R. J. (2009) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2009.07.030 · Cited by 62
The indoleamine 2,3‐dioxygenase ( IDO ) pathway controls allergy
von Bubnoff, D., & Bieber, T. R. M. (2012) · Allergy · doi:10.1111/j.1398-9995.2012.02830.x · Cited by 61
Taglauer, E. S., Waldorf, K. M. A., & Petroff, M. G. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082800et · Cited by 60
Microchimerism and the pathogenesis of systemic sclerosis
Nelson, J. L. (1998) · Current Opinion in Rheumatology · doi:10.1097/00002281-199811000-00010 · Cited by 59
2 The normal fetomaternal immune relationship
Billington, W. D. (1992) · Baillière s Clinical Obstetrics and Gynaecology · doi:10.1016/s0950-3552(05)80004-5 · Cited by 59
Neuroendocrine-Immune Interactions in Rheumatoid Arthritis: Mechanisms of Glucocorticoid Resistance
Silverman, M. N., & Sternberg, E. M. (2008) · NeuroImmunoModulation · doi:10.1159/000135620 · Cited by 57
Maternal vitamin D deficiency: Fetal and neonatal implications
Kovács, C. S. (2013) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2013.01.005 · Cited by 57
Caserta, M. T., Wyman, P. A., Wang, H., Moynihan, J. A., & O’Connor, T. G. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000526 · Cited by 48
Self-citationSession 1: Allergic disease Nutrition as a potential determinant of asthma
Devereux, G. S. (2009) · Proceedings of The Nutrition Society · doi:10.1017/s0029665109991753 · Cited by 46
Maternal Vitamin D Supplementation to Meet the Needs of the Breastfed Infant
Thiele, D. K., Senti, J. L., & Anderson, C. M. (2013) · Journal of Human Lactation · doi:10.1177/0890334413477916 · Cited by 45
The Promise of Epidemiologic Studies: Neuroimmune Mechanisms in the Etiologies of Brain Disorders
Ellman, L. M., & Susser, E. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.024 · Cited by 43
Self-citationGlucocorticoids and the Th1/Th2 Balance
(2003) · Hormone and Metabolic Research · doi:10.1055/s-2003-43512-15 · Cited by 43
Coulon, M., Wellman, C. L., Marjara, I. S., Janczak, A. M., & Zanella, A. J. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.10.018 · Cited by 40
Hematopoiesis and Retinoids: Development and Disease
Oren, T., Sher, J., & Evans, T. (2003) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/1042819031000116661 · Cited by 39
Maternal depression related to infant’s wheezing
Lefèvre, F., Moreau, D., Sémon, E., Kalaboka, S., Annesi‐Maesano, I., & Just, J. (2011) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2011.01155.x · Cited by 38
Elevated C-Reactive Protein in Adolescents
Low, C. A., Matthews, K. A., & Hall, M. H. (2013) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31828d3f1d · Cited by 38
Robinson, M. J., Heal, C., Gardener, E. A., Powell, P. J., & Sims, D. G. (2004) · PEDIATRICS · doi:10.1542/peds.113.4.733 · Cited by 37
No Moderating Effect of 5-HTTLPR on Associations Between Antenatal Anxiety and Infant Behavior
Braithwaite, E., Ramchandani, P. G., O’Connor, T. G., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Glover, V. A. S., Netsi, E., Evans, J., Meaney, M. J., & Murphy, S. E. (2013) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.02.010 · Cited by 34
Self-citationBreckler, L., Hale, J., Taylor, A. L., Dunstan, J. A., Thornton, C. A., & Prescott, S. L. (2008) · Allergy · doi:10.1111/j.1398-9995.2008.01718.x · Cited by 33
Inflammation and diminished iron status: mechanisms and functional outcomes
Gaffney-Stomberg, E., & McClung, J. P. (2012) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e328357f63b · Cited by 33
Okoko, B. J., Wesumperuma, L. H., & Hart, A. C. (2001) · Vaccine · doi:10.1016/s0264-410x(01)00418-2 · Cited by 32
Prenatal determinants of schizophrenia: what we have learned thus far?
Bresnahan, M. A., Schaefer, C. A., Brown, A. S., & Susser, E. (2005) · Epidemiology and Psychiatric Sciences · doi:10.1017/s1121189x00007946 · Cited by 24
Self-citationBreckler, L., Hale, J., Jung, W., Westcott, L., Dunstan, J. A., Thornton, C. A., & Prescott, S. L. (2009) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2009.00880.x · Cited by 22
Perinatal Stress Influences Lymphocyte Subset Counts in Neonates. The Generation R Study
Duijts, L., Bakker‐Jonges, L. E., Labout, J. A. M., Jaddoe, V. W. V., Albert Hofman, D., Steegers, E. A. P., van Dongen, J. J. M., Hooijkaas, H., & Moll, H. A. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e318163a29f · Cited by 21
Prescott, S. L., Breckler, L., Witt, C. S., Smith, L., Dunstan, J. A., & Christiansen, F. (2009) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2009.04042.x · Cited by 21
Development of the Human Immune System
Leibnitz, R. (2004) · Informa Healthcare eBooks · doi:10.1201/9781420024036.ch2 · Cited by 17
Can maternal microchimeric cells influence the fetal response toward self antigens?
Leveque, L., & Khosrotehrani, K. (2011) · Chimerism · doi:10.4161/chim.17589 · Cited by 15
Can maternal microchimeric cells influence the fetal response toward self antigens?
Leveque, L., & Khosrotehrani, K. (2011) · PubMed · doi:10.4161/chim.2.3.17589 · Cited by 12
Oh, S., Zheng, T., Bailey, M., et al. (2007) · Open Access System for Information Sharing (Pohang University of Science and Technology) · doi:10.1016/j.jaci.2006 · Cited by 9
Relating the Effects of Prenatal Stress in Rodents to the Pathogenesis of Schizophrenia
Moore, H. M., & Susser, E. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.001 · Cited by 8
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- Brown A. S. Cohen P. Greenwald S. Susser E. McCann J. C. Ames B. N. (2000b). Nonaffective psychosis after prenatal exposure to rubella An overview of evidence for a causal relation between iron deficiency during development and deficits in cognitive or behavioral function Iron fortification of foods: overcoming technical and practical barriers ACOG Practice Bulletin No. 95, anemia pregnancy Identifying window vulnerability during fetal development maternal iron restriction model. Am. J. Psychiatry 157, 438– 443 10.1176/appi.ajp.157.3.438 10698821 · DOI
- Chaouat G. Menu R. Kinsky M. Dy M. Delage M. N. Thang D. A. (1990). Lymphokines and nin-specific cellular lytic effectors at the feto-matrnal interface affect placental size and survival, in Reproductive Immunology, eds Mettler L. Billington D. (Amsterdam: Elsevier Science Ltd).
Cited by
Sorted by citations
Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089
From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways
Rogers, G. B., Keating, D. J., Young, R. L., Wong, M.-L., Licinio, J., & Wesselingh, S. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.50 · Cited by 969
Immune Dysfunction as a Cause and Consequence of Malnutrition
Bourke, C. D., Berkley, J. A., & Prendergast, A. J. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.04.003 · Cited by 771
Paolicelli, R. C., & Ferretti, M. T. (2017) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2017.00009 · Cited by 252
Hardy, A., Benford, D., Halldorsson, T. I., Jeger, M. J., Knutsen, H. K., More, S. J., Naegeli, H., Noteborn, H. P. J. M., Ockleford, C., Ricci, A., et al. (2017) · EFSA Journal · doi:10.2903/j.efsa.2017.4849 · Cited by 210
Metadata
- Authors
- Marques, A. H., O'Connor, T. G., Roth, C., Susser, E., & Bjørke-Monsen, A.-L.
- Affiliations
- Columbia University (US)
- Norwegian Institute of Public Health (NO)
- New York State Psychiatric Institute (US)
- Corresponding author
- Marques, Andrea Horvath
- ORCID
- Susser, Ezra
- Venue
- Frontiers in Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2013
- Volume
- 7
- Pages
- 120-120
- ISSN
- 1662-453X (ISSN-L)
- PMC
- PMC3728489
- OpenAlex
- W2116510315
- Cited by
- 226
- References
- 238
- Citations by year
- 2026: 18 · 2025: 16 · 2024: 19 · 2023: 10 · 2022: 22 · 2021: 24 · 2020: 21 · 2019: 11 · 2018: 17 · 2017: 21 · 2016: 20 · 2015: 12 · 2014: 12 · 2013: 3
- FWCI
- 14.58
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- GRO (submittedVersion, cc-by)
- Funders
- National Institute of Mental Health (R01MH073019)
- National Institute of Diabetes and Digestive and Kidney Diseases (T32DK091227)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- 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
- Keywords
- maternal nutrition, prenatal nutrition, infant nutrition, maternal stress, maternal anxiety, fetal immune system development, neurodevelopmental disorders, autism spectrum disorder, schizophrenia, maternal-fetal immune interaction, micronutrient supplementation
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