Cited by 262Autism Spectrum Disorder ResearchTryptophan and brain disordersGenetics and Neurodevelopmental Disorders

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Neonatal Cytokine Profiles Associated With Autism Spectrum Disorder

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Krakowiak, Paula, Goines, Paula E., Tancredi, Daniel J., Ashwood, Paul, Hansen, Robin L., Hertz-Picciotto, Irva, Van de Water, Judy·2017·Biological Psychiatry

DOI 10.1016/j.biopsych.2015.08.007PMC PMC4753133

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Abstract

Background Autism spectrum disorder (ASD) is a complex neurodevelopmental condition that can be reliably diagnosed at age 24 months. Immunological phenomena, including skewed cytokine production, have been observed among children with ASD. Little is known about whether immune dysregulation is present before diagnosis of ASD.Methods We examined neonatal blood spots from 214 children with ASD (141 severe, 73 mild/moderate), 62 children with typical development, and 27 children with developmental delay as control subjects who participated in the Childhood Autism Risks from Genetics and the Environment study, a population-based case-control study. Levels of 17 cytokines and chemokines were compared across groups and in relation to developmental and behavioral domains.Results Interleukin (IL)-1β and IL-4 were independently associated with ASD compared with typical development, although these relationships varied by ASD symptom intensity. Elevated IL-4 was associated with increased odds of severe ASD (odds ratio [OR] = 1.40, 95% confidence interval [CI], 1.03, 1.91), whereas IL-1β was associated with increased odds of mild/moderate ASD (OR = 3.02, 95% CI, 1.43, 6.38). Additionally, IL-4 was associated with a higher likelihood of severe ASD versus mild/moderate ASD (OR = 1.35, 95% CI, 1.04, 1.75). In male subjects with ASD, IL-4 was negatively associated with nonverbal cognitive ability (β = -3.63, SE = 1.33, p = .04).Conclusions This study is part of a growing effort to identify early biological markers for ASD. We demonstrate that peripheral cytokine profiles at birth are associated with ASD later in childhood and that cytokine profiles vary depending on ASD severity. Cytokines have complex roles in neurodevelopment, and dysregulated levels may be indicative of genetic differences and environmental exposures or their interactions that relate to ASD.

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“(18) found that levels of several cytokines, including interleukin (IL) -1ß and IL-4, are elevated at birth in individuals with ASD compared to typically developing controls.”
Background
TREM2 improves microglia function and synaptic development in autism spectrum disorders by regulating P38 MAPK signaling pathway
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Background
Fetal-placental crosstalk occurs through fetal cytokine synthesis and placental clearance
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“Also, elevated levels of IL-1β, IL-4, IL-6 or IL-8 in dried blood spots collected after birth increase the risk of later ASD diagnosis [9, 10].”
Background
TH1/Treg ratio may be a marker of autism in children with immune dysfunction
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“Furthermore, altered immune function is frequently observed in children with ASD (Meltzer and Van De Water, 2017), including cytokine dysregulation (Goines and Ashwood, 2013; Masi et al., 2015), and may be contributing factors in the pathogenesis of these disorders, which exhibit a strong sex bias…”
Background
Maternal Gestational Immune Response and Autism Spectrum Disorder Phenotypes at 7 Years of Age in the Seychelles Child Development Study
Irwin, J. L., Yeates, A. J., Mulhern, M. S., McSorley, E. M., Strain, J., Watson, G. E., Grzesik, K., Thurston, S. W., Love, T., Smith, T. H., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1424-y · Cited by 20
Prenatal Influenza Vaccination or Influenza Infection and Autism Spectrum Disorder in Offspring
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“…differentially expressed genes common between ASD and Non-TD revealed enrichment for the interferon-gamma mediated signaling pathway, which has been previously found to be elevated in mothers of children with ASD and other neurodevelopmental disorders [Goines et al., 2011; Krakowiak et al., 2017].”
BackgroundSelf-citation
Toward a better understanding of T cell dysregulation in autism: An integrative review
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“In a separate study using the Childhood Autism Risks from Genetics and the Environment (CHARGE) cohort, elevated IL-1 β and IL-4 in neonatal blood spots was associated with moderate and severe ASD (Krakowiak, 2017).”
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Acetaminophen Use for Fever in Children Associated with Autism Spectrum Disorder
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“Recent studies have identified several immune responses, such as higher concentrations of intergerons in ASD-ID versus the general population, or ASD alone [32,45].”
Background
How 25(OH)D Levels during Pregnancy Affect Prevalence of Autism in Children: Systematic Review
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“That increase is strongly associated with cognitive impairment in ASD [52].”
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DAPTA, a C-C chemokine receptor 5 (CCR5) antagonist attenuates immune aberrations by downregulating Th9/Th17 immune responses in BTBR T+ Itpr3tf/J mice
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What does immunology have to do with brain development and neuropsychiatric disorders?
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“IL-4 levels in neonates were associated with ASD development and symptom severity in later childhood [Krakowiak et al., 2017].”
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Moderate prenatal alcohol exposure suppresses the TLR4-mediated innate immune response in the hippocampus of young rats
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“Altered cytokine profiles have been consistently reported in subjects with ASD, including in the neonatal period (Krakowiak et al., 2017; Masi et al., 2017; Eftekharian et al., 2018).”
Elevated levels of peripheral and central nervous system immune markers reflect innate immune dysregulation in autism spectrum disorder
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Ashwood, P. (2023) · Biomedicines · doi:10.3390/biomedicines11020436 · Cited by 14
“Increased IL-4 has also been found in neonatal blood spots from children who later developed severe AU [49].”
BackgroundSelf-citation
A potent and selective CXCR2 antagonist improves neuroimmune dysregulation through the inhibition of NF-κB and notch inflammatory signaling in the BTBR mouse model of autism
Alomar, H. A., Ansari, M. A., Nadeem, A., Attia, S. M., Bakheet, S. A., Al‐Mazroua, H. A., Hussein, M. H., Alqarni, S. A., & Ahmad, S. F. (2023) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2023.578069 · Cited by 15
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Background
Immune activity at birth and later psychopathology in childhood
Barbosa, S., Khalfallah, O., Forhan, A., Galéra, C., Heude, B., Glaichenhaus, N., & Davidovic, L. (2020) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2020.100141 · Cited by 14
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Associations between the human immune system and gut microbiome with neurodevelopment in the first 5 years of life: A systematic scoping review
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Socio-economic status and autism spectrum disorder: A case-control study in Bangladesh
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“…the male gender was highly significant (BLR, MLR, FLR) and increased > twofold odds of ASD compared to HC which is in similar line with several previous studies (Krakowiak et al., 2015; Oommen et al., 2018; Maia et al., 2019; Soke et al., 2019; Gil-Hern ´ andez et al., 2020; Hegazy et al., 2021).”
Result
Upregulation of Inflammatory Mediators in Peripheral Blood CD40+ Cells in Children with Autism Spectrum Disorder
Aldossari, A. A., Ansari, M. A., Nadeem, A., Attia, S. M., Bakheet, S. A., AL-Ayadhi, L. Y., Alanazi, M. M., Shahid, M., Alwetaid, M. Y., Hussein, M. H., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087475 · Cited by 13
“Altered immune responses commonly occur in individuals genetically susceptible to ASD [51,52].”
Background
How does autism spectrum disorder affect the risk and severity of childhood asthma?
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The Association of Prenatal Tetanus, Diphtheria, and Acellular Pertussis (Tdap) Vaccination With Attention-Deficit/Hyperactivity Disorder
Becerra-Culqui, T. A., Getahun, D. T., Chiu, V. Y., Sy, L. S., & Tseng, H. F. (2020) · American Journal of Epidemiology · doi:10.1093/aje/kwaa074 · Cited by 13
Rapid Communication: Plasma Interleukin-35 in Children with Autism
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Self-citation
Adolescent swimming exercise following maternal valproic acid treatment improves cognition and reduces stress-related symptoms in offspring mice: Role of sex and brain cytokines
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A Putative Blood-Based Biomarker for Autism Spectrum Disorder-Associated Ileocolitis
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Mast Cells in Autism Spectrum Disorder—The Enigma to Be Solved?
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“Elevated IL-4 is associated with higher severity of ASD, while excessive IL-1 β is linked to a milder form of the disease [122].”
Background
Associations Among Maternal Metabolic Conditions, Cord Serum Leptin Levels, and Autistic Symptoms in Children
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“Covariates We included children’s sex, maternal age at delivery, educational attainment of mothers, household income at birth, gestational age at birth (<37 or≥37 weeks), birth weight, maternal smoking status during pregnancy, andmode of feeding during 0–6months of age (breastfeeding only, formula only, breastfeeding,…”
Method
Intra-amniotic inflammation in the mid-trimester of pregnancy is a risk factor for neuropsychological disorders in childhood
Gervasi, M. T., Romero, R. J., Cainelli, E., Veronese, P., Tran, M. R., Jung, E., Suksai, M., Bosco, M., & Gotsch, F. (2022) · Journal of Perinatal Medicine · doi:10.1515/jpm-2022-0255 · Cited by 12
Pre-autism: What a paediatrician should know about early diagnosis of autism
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“Another study by Krakowiak et al [154] showed that high neonatal levels of IL-1 β are associated with an increased risk of mild to moderate autism.”
Maternal atopic conditions and autism spectrum disorder: a systematic review
Şeker, A., Gurakuqi, A. Q., Tabaku, M., Javate, K. R., & Carcani-Rathwell, I. (2023) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-023-02285-7 · Cited by 13
“…supported by studies demonstrating increased cytokine levels in midg-estational serum of mothers of offspring with ASD [53], as well as in amniotic fluid [54], and newborn blood spots of children eventually diagnosed with ASD [55], although levels of specific cytokines vary in each experiment.”
The Immune/Inflammatory Underpinnings of Neurodevelopmental Disorders and Pediatric Acute-Onset Neuropsychiatric Syndrome: A Scoping Review
Gagliano, A., Cucinotta, F., Giunta, I., Modica, I. D., Domenico, C. D., Costanza, C., Germanò, E., & Frankovich, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26167767 · Cited by 14
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Plasma cytokine concentrations of children with autism spectrum disorder and neurotypical siblings
Belica, I., Janšáková, K., Celušáková, H., Kopčíková, M., Polónyiová, K., Rašková, B., Vidošovičová, M., Ostatníková, D., & Babinská, K. (2023) · Cytokine · doi:10.1016/j.cyto.2023.156333 · Cited by 11
Regional skull translocator protein elevation in autistic adults detected by PET-MRI
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Preterm Birth by Cesarean Section: The Gut-Brain Axis, a Key Regulator of Brain Development
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Identifying Rare Genetic Variants of Immune Mediators as Risk Factors for Autism Spectrum Disorder
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“[30,64]; in recent years, researchers have begun to focus on the discovery of maternal autoantibodies [18,21–23,25,26] and understanding the role of gut microbiota in it [65–67].”
Background
Chemical Modulators for Targeting Autism Spectrum Disorders: From Bench to Clinic
Lim, S., & Lee, S. (2022) · Molecules · doi:10.3390/molecules27165088 · Cited by 9
The relationship of immune cells with autism spectrum disorder: a bidirectional Mendelian randomization study
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“On the other hand, the current research has shown contradictory conclusions regarding the connection between immunological inflammation and ASD [10].”
Background
Crosstalk Between Mitochondrial DNA and Immune Response: Focus on Autism Spectrum Disorder
Qu, W., Yan, G., Du, Y., Zhou, X., Huang, C., Li, B., Zhou, J., & Li, Q. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04637-z · Cited by 8
“Additionally, increased levels of IL-1β and IL-4 in newborn blood have been linked to more severe forms of ASD [19].”
Genetic variants drive altered epigenetic regulation of endotoxin response in BTBR macrophages
Ciernia, A. V., Link, V. M., Careaga, M., LaSalle, J. M., & Ashwood, P. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.05.058 · Cited by 8
Self-citation
Modifiable Nutritional Biomarkers in Autism Spectrum Disorder: A Systematic Review and Meta-Analysis of Vitamin D, B12, and Homocysteine Exposure Spanning Prenatal Development Through Late Adolescence
Avram, O.-E., Bratu, E.-A., Curis, C., Moroianu, L.-A., & Drima, E. P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26094410 · Cited by 14
Complement system dysfunction in autism spectrum disorder: evidence for altered C1q and C3 levels (complement system dysfunction in ASD)
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“One study reported that infections during pregnancy increase the risk of ASD through maternal immune activation (Jiang et al. , 2016; Krakowiak et al. , 2017).”
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BackgroundInfluential
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The effects of parental occupational exposures on autism spectrum disorder severity and skills in cognitive and adaptive domains in children with autism spectrum disorder
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Assessing for prenatal risk factors associated with infant neurologic morbidity using a multivariate analysis
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Authors: Krakowiak, P., Goines, P. E., Tancredi, D. J., Ashwood, P., Hansen, R. L., Hertz-Picciotto, I., & Van de Water, J.
Affiliations: University of California, Davis (US)
ORCID: Krakowiak, Paula
Tancredi, Daniel J.
Ashwood, Paul
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2017-03
Volume: 81
Issue: 5
Pages: 442-451
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2015.08.007
PMC: PMC4753133
OpenAlex: W1409858176
Cited by: 249
References: 65
Citations by year: 2026: 15 · 2025: 14 · 2024: 34 · 2023: 32 · 2022: 35 · 2021: 16 · 2020: 27 · 2019: 26 · 2018: 28 · 2017: 12
FWCI: 10.02
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (P01 ES11269 and R01 ES015359)
U.S. Environmental Protection Agency through the Science to Achieve Results (STAR) (R829388, R833292)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: autism spectrum disorder, IL-1β, IL-4, immune dysregulation, ASD severity, biomarkers, nonverbal cognitive ability, developmental delay, chemokines, brain development
MeSH terms: Autism Spectrum Disorder, Child, Preschool, Female, Humans, Male, Severity of Illness Index, Biomarkers, Interleukin-4, Case-Control Studies, Cytokines, Interleukin-1beta

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Neonatal Cytokine Profiles Associated With Autism Spectrum Disorder

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