Journal of Autism and Developmental Disorders

, Volume 48, Issue 8, pp 2766–2778 | Cite as

Maternal Exposures Associated with Autism Spectrum Disorder in Jamaican Children

  • MacKinsey A. Christian
  • Maureen Samms-Vaughan
  • MinJae Lee
  • Jan Bressler
  • Manouchehr Hessabi
  • Megan L. Grove
  • Sydonnie Shakespeare-Pellington
  • Charlene Coore Desai
  • Jody-Ann Reece
  • Katherine A. Loveland
  • Eric Boerwinkle
  • Mohammad H. RahbarEmail author
Original Paper


Autism spectrum disorder (ASD) is a complex neurodevelopmental disorder with poorly understood etiology. Many maternal exposures during pregnancy and breastfeeding potentially interfere with neurodevelopment. Using data from two age- and sex-matched case-control studies in Jamaica (n = 298 pairs), results of conditional logistic regression analyses suggest that maternal exposures to fever or infection (matched odds ratio (MOR) = 3.12, 95% CI 1.74–5.60), physical trauma (MOR 2.02, 95% CI 1.01–4.05), and oil-based paints (MOR 1.99, 95% CI 1.14–3.46) may be associated with ASD. Additionally, maternal exposure to oil-based paints may modify the relationship between maternal exposure to pesticides and ASD, which deepens our understanding of the association between pesticides and ASD.


Fever Physical trauma Volatile organic compounds Pesticides Autism spectrum disorder Jamaica 



This research is co-funded by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) and the National Institutes of Health Fogarty International Center (NIH-FIC) by a grant (R21HD057808) as well as National Institute of Environmental Health Sciences (NIEHS) by a grant (R01ES022165) awarded to The University of Texas Health Science Center at Houston. We also acknowledge the support provided by the Biostatistics/Epidemiology/Research Design (BERD) component of the Center for Clinical and Translational Sciences (CCTS) for this project. CCTS is mainly funded by the NIH Centers for Translational Science Award (NIH CTSA) grant (UL1 RR024148), awarded to The University of Texas Health Science Center at Houston in 2006 by the National Center for Research Resources (NCRR) and its renewal (UL1 TR000371) by the National Center for Advancing Translational Sciences (NCATS). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NICHD or the NIH-FIC or NIEHS or the NCRR or the NCATS. This manuscript was prepared from the Master’s thesis completed by MacKinsey A. Christian.

Author Contributions

MAC was primarily responsible for analyzing the data, interpreting the findings, and drafting the manuscript. MHR is Principal Investigator (PI) of the ERAJ and ERAJ-2 studies from which these data originated and is responsible for designing and obtaining funding for these studies. MHR also served as chair of MAC’s thesis committee, and participated in interpreting the findings and revising the manuscript. MSV is co-investigator and PI of subcontract to the UWI for the ERAJ and ERAJ-2 studies and is responsible for designing the study and providing oversight to our study team in Jamaica. MSV also participated in revising the manuscript. MLG served on MAC’s thesis committee and participated in interpreting the findings and revising the manuscript. JB, KAL, and EB are co-Investigators of the ERAJ and ERAJ-2 studies who contributed to study design and participated in revising the manuscript. MH is responsible for data management of the ERAJ and ERAJ-2 studies and participated in revising the manuscript. MLG contributed to study design and participated in revising the manuscript. SSP is responsible for data collection and participated in revising the manuscript. CCD is responsible for coordinating study activities in Jamaica and participated in revising the manuscript. JAR is responsible for data entry and participated in revising the manuscript. All authors approved the final version.

Compliance with Ethical Standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. Adair-Kirk, T. L., Atkinson, J. J., Kelley, D. G., Arch, R. H., Miner, J. H., & Senior, R. M. (2005). A chemotactic peptide from laminin alpha 5 functions as a regulator of inflammatory immune responses via TNF alpha-mediated signaling. Journal of immunology, 174(3), 1621–1629.CrossRefGoogle Scholar
  2. Agran, P. F., Dunkle, D. E., Winn, D. G., & Kent, D. (1987). Fetal death in motor vehicle accidents. Annals of Emergency Medicine, 16(12), 1355–1358.CrossRefPubMedGoogle Scholar
  3. Alobuia, W. M., Missikpode, C., Aung, M., & Jolly, P. E. (2015). Knowledge, attitude, and practices regarding vector-borne diseases in Western Jamaica. Annals of Global Health, 81(5), 654–663.CrossRefPubMedPubMedCentralGoogle Scholar
  4. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5-«) Washington, DC: American Psychiatric Pub.CrossRefGoogle Scholar
  5. Arscott-Mills, S., Gordon, G., McDonald, A., Holder, Y., & Ward, E. (2002). A profile of injuries in Jamaica. Injury Control and Safety Promotion, 9(4), 227–234.CrossRefPubMedGoogle Scholar
  6. Atladottir, H. O., Henriksen, T. B., Schendel, D., Schendel, D. E., Parner, E. T. (2012). Autism after infection, febrile episodes, and antibiotic use during pregnancy: An exploratory study. Pediatrics, 130(6), 1447–1454.CrossRefGoogle Scholar
  7. Atladottir, H. O., Thorsen, P. F., Ostergaard, L. F., Schendel, D. E. F. A. U., - Lemcke, S., Lemcke, S. F. A. U., - Abdallah, M., Abdallah, M. F., et al. (2010). Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. Journal of Autism and Developmental Disorders, 40(12), 1423–1430.CrossRefPubMedGoogle Scholar
  8. Austim and Developmental Disabilities Monitoring Network Surveillance Year 2010 Principal Investigators (2014). Prevalence of autism spectrum disorder among children aged 8 years-autism and developmental disabilities monitoring network, 11 sites, United States, 2010. Morbidity and Mortality Weekly Report: Surveillance Summaries, 63(2), 1–21.Google Scholar
  9. Baethmann, M., Kahn, T., Lenard, H. G., & Voit, T. (1996). Fetal CNS damage after exposure to maternal trauma during pregnancy. Acta Paediatrica, 85(11), 1331–1338.CrossRefPubMedGoogle Scholar
  10. Bari, M. A., & Kindzierski, W. B. (2017). Concentrations, sources and human health risk of inhalation exposure to air toxics in Edmonton, Canada. Chemosphere, 173, 160–171.CrossRefPubMedGoogle Scholar
  11. Boyle, E. B., Viet, S. M., Wright, D. J., Merrill, L. S., Alwis, K. U., Blount, B. C., et al. (2016). Assessment of exposure to VOCs among pregnant women in the National Children’s Study. International Journal of Environmental Research and Public Health, 13(4), 376.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Breysem, L., Cossey, V., Mussen, E., Demaerel, P., Van de Voorde, W., & Smet, M. (2004). Fetal trauma: brain imaging in four neonates. European Radiology, 14(9), 1609–1614.CrossRefPubMedGoogle Scholar
  13. Brown, H. S., Bishop, D. R., & Rowan, C. A. (1984). The role of skin absorption as a route of exposure for volatile organic compounds (VOCs) in drinking water. American Journal of Public Health, 74(5), 479–484.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Brown, M. G., Vickers, I. E., Salas, R. A., & Smikle, M. F. (2009). Seroprevalence of dengue virus antibodies in healthy Jamaicans. Human Antibodies, 18(4), 123–126.CrossRefPubMedGoogle Scholar
  15. Budday, S., Steinmann, P., & Kuhl, E. (2015). Physical biology of human brain development. Frontiers in Cellular Neuroscience, 9, 257CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chibber, R., Al-Harmi, J., Fouda, M., & El-Saleh, E. (2015). Motor-vehicle injury in pregnancy and subsequent feto-maternal outcomes: Of grave concern. Journal of Maternal-Fetal & Neonatal Medicine, 28(4), 399–402.CrossRefGoogle Scholar
  17. Choi, G. B., Yim, Y. S., Wong, H., Kim, S., Kim, H., Kim, S. V., et al. (2016). The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science, 351(6276), 933–939.CrossRefPubMedPubMedCentralGoogle Scholar
  18. D’Amelio, M., Ricci, I., Sacco, R., Liu, X., D’Agruma, L., Muscarella, L. A., et al. (2005). Paraoxonase gene variants are associated with autism in North America, but not in Italy: Possible regional specificity in gene-environment interactions. Molecular Psychiatry, 10(11), 1006–1016.CrossRefPubMedGoogle Scholar
  19. Dassa, D., Takei, N., Sham, P. C., & Murray, R. M. (1995). No association between prenatal exposure to influenza and autism. Acta Psychiatrica Scandinavica, 92(2), 145–149.CrossRefPubMedGoogle Scholar
  20. De Felice, A., Greco, A., Calamandrei, G., & Minghetti, L. (2016). Prenatal exposure to the organophosphate insecticide chlorpyrifos enhances brain oxidative stress and prostaglandin E 2 synthesis in a mouse model of idiopathic autism. Journal of Neuroinflammation, 13(1), 149.CrossRefPubMedPubMedCentralGoogle Scholar
  21. De Felice, A., Scattoni, M. L., Ricceri, L., & Calamandrei, G. (2015). Prenatal exposure to a common organophosphate insecticide delays motor development in a mouse model of idiopathic autism. PLoS One, 10(3), e0121663.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dewailly, E., Forde, M., Robertson, L., Kaddar, N., Sidi, E. A. L., Cote, S., et al. (2014). Evaluation of pyrethroid exposures in pregnant women from 10 Caribbean countries. Environment International, 63, 201–206.CrossRefPubMedGoogle Scholar
  23. Domingues, V. F., Nasuti, C., Piangerelli, M., Correia-Sa, L., Ghezzo, A., Marini, M., et al. (2016). Pyrethroid pesticide metabolite in urine and microelements in hair of children affected by autism spectrum disorders: A preliminary investigation. International Journal of Environmental Research and Public Health, 13(4), 388.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Estes, M. L., & McAllister, A. K. (2015). Immune mediators in the brain and peripheral tissues in autism spectrum disorder. Nature Reviews Neuroscience, 16(8), 469–486.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fernandez, A., Singh, A., & Jaffe, R. (2007). A literature review on trace metals and organic compounds of anthropogenic origin in the Wider Caribbean Region. Marine Pollution Bulletin, 54(11), 1681–1691.CrossRefPubMedGoogle Scholar
  26. Forde, M. S., Robertson, L., Sidi, E. A. L., Cote, S., Gaudreau, E., Drescher, O., et al. (2015). Evaluation of exposure to organophosphate, carbamate, phenoxy acid, and chlorophenol pesticides in pregnant women from 10 Caribbean countries. Environmental Science: Processes & Impacts, 17(9), 1661–1671.Google Scholar
  27. Grether, J. K., Ashwood, P., Van de Water, J., Yolken, R. H., Anderson, M. C., Torres, A. R., et al. (2016). Prenatal and newborn immunoglobulin levels from mother–child pairs and risk of autism spectrum disorders. Frontiers in Neuroscience, 10, 218CrossRefPubMedPubMedCentralGoogle Scholar
  28. Herzine, A., Laugeray, A., Feat, J., Menuet, A., Quesniaux, V., Richard, O., et al. (2016). Perinatal exposure to glufosinate ammonium herbicide impairs neurogenesis and neuroblast migration through cytoskeleton destabilization. Front Cell Neuroscience, 10, 191. Scholar
  29. Hjortebjerg, D., Andersen, A. M., Garne, E., Raaschou-Nielsen, O., & Sorensen, M. (2012). Non-occupational exposure to paint fumes during pregnancy and risk of congenital anomalies: A cohort study. Environmental Health, 11, 54.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hsiao, E. Y., McBride, S. W., Chow, J., Mazmanian, S. K., & Patterson, P. H. (2012). Modeling an autism risk factor in mice leads to permanent immune dysregulation. Proceedings of the National Academy of Sciences of the United States of America, 109(31), 12776–12781.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Juul-Dam, N., Townsend, J. F., & Courchesne, E. (2001). Prenatal, perinatal, and neonatal factors in autism, pervasive developmental disorder-not otherwise specified, and the general population. Pediatrics, 107(4), E63.CrossRefPubMedGoogle Scholar
  32. Kalkbrenner, A. E., Daniels, J. L., Chen, J. C., Poole, C., Emch, M., & Morrissey, J. (2010). Perinatal exposure to hazardous air pollutants and autism spectrum disorders at age 8. Epidemiology, 21(5), 631–641.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kalkbrenner, A. E., Schmidt, R. J., & Penlesky, A. C. (2014). Environmental chemical exposures and autism spectrum disorders: A review of the epidemiological evidence. Current Problems in Pediatric and Adolescent Health Care, 44(10), 277–318.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Keil, A. P., Daniels, J. L., & Hertz-Picciotto, I. (2014). Autism spectrum disorder, flea and tick medication, and adjustments for exposure misclassification: the CHARGE (CHildhood Autism Risks from Genetics and Environment) case-control study. Environmental Health, 13(1), 3.Google Scholar
  35. Khan, N. Z., Gallo, L. A., Arghir, A., Budisteanu, B., Budisteanu, M., Dobrescu, I., et al. (2012). Autism and the grand challenges in global mental health. Autism Research, 5(3), 156–159.CrossRefPubMedGoogle Scholar
  36. Langridge, A. T., Glasson, E. J., Nassar, N., Jacoby, P., Pennell, C., Hagan, R., et al. (2013). Maternal conditions and perinatal characteristics associated with autism spectrum disorder and intellectual disability. PLoS ONE, 8(1), e50963.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Laslo-Baker, D., Barrera, M., Knittel-Keren, D., Kozer, E., Wolpin, J., Khattak, S., et al. (2004). Child neurodevelopmental outcome and maternal occupational exposure to solvents. Archives of Pediatrics & Adolescent Medicine, 158(10), 956–961.CrossRefGoogle Scholar
  38. Laugeray, A., Herzine, A., Perche, O., Hebert, B., Aguillon-Naury, M., Richard, O., et al. (2014). Pre- and postnatal exposure to low dose glufosinate ammonium induces autism-like phenotypes in mice. Frontiers in Behavioral Neuroscience, 8, 390. Scholar
  39. Le Belle, J. E., Sperry, J., Ngo, A., Ghochani, Y., Laks, D. R., Lopez-Aranda, M., et al. (2014). Maternal inflammation contributes to brain overgrowth and autism-associated behaviors through altered redox signaling in stem and progenitor cells. Stem Cell Reports, 3(5), 725–734.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lee, B. K., Magnusson, C., Gardner, R. M., Blomstrom, A., Newschaffer, C. J., Burstyn, I., et al. (2015). Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders. Brain, Behavior, and Immunity, 44, 100–105.CrossRefPubMedGoogle Scholar
  41. Lee, I., Eriksson, P., Fredriksson, A., Buratovic, S., & Viberg, H. (2015). Developmental neurotoxic effects of two pesticides: Behavior and neuroprotein studies on endosulfan and cypermethrin. Toxicology, 335, 1–10.CrossRefPubMedGoogle Scholar
  42. Lewis-Bell, K., Luciani, S., Unger, E. R., Hariri, S., McFarlane, S., Steinau, M., et al. (2013). Genital human papillomaviruses among women of reproductive age in Jamaica. Revista Panamericana de Salud Publica, 33(3), 159–165.CrossRefPubMedGoogle Scholar
  43. Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. L. (1999). Autism diagnostic observation schedule (ADOS) manual. Los Angeles, CA: Western Psychological Services.Google Scholar
  44. Lyall, K., Croen, L., Daniels, J., Fallin, M. D., Ladd-Acosta, C., Lee, B. K., et al. (2017a). The changing epidemiology of autism spectrum disorders. Annual Review of Public Health, 38, 81–102. Scholar
  45. Lyall, K., Croen, L. A., Sjodin, A., Yoshida, C. K., Zerbo, O., Kharrazi, M., et al. (2017b). Polychlorinated biphenyl and organochlorine pesticide concentrations in maternal mid-pregnancy serum samples: Association with autism spectrum disorder and intellectual disability. Environmental Health Perspectives, 125(3), 474–480. Scholar
  46. Martinez-Alfaro, M., Carabez-Trejo, A., Sandoval-Zapata, F., Morales-Tlalpan, V., & Palma-Tirado, L. (2014). Subsurface cistern (SSC) proliferation in Purkinje cells of the rat cerebellum in response to acute and chronic exposure to paint thinner: A light and electron microscopy study. Experimental and Toxicologic Pathology, 66(7), 323–332.CrossRefPubMedGoogle Scholar
  47. McCaw-Binns, A., Ashley, D., Samms-Vaughan, M., Wilks, R., Ferguson, T., Younger, N., et al. (2011). Cohort profile: The Jamaican 1986 birth cohort study. International Journal of Epidemiology, 40(6), 1469–1476.CrossRefPubMedGoogle Scholar
  48. McDougle, C. J., Landino, S. M., Vahabzadeh, A., O’Rourke, J., Zurcher, N. R., Finger, B. C., et al. (2015). Toward an immune-mediated subtype of autism spectrum disorder. Brain Research, 1617, 72–92.CrossRefPubMedGoogle Scholar
  49. Millenson, M. E., Braun, J. M., Calafat, A. M., Barr, D. B., Huang, Y. T., Chen, A., et al. (2017). Urinary organophosphate insecticide metabolite concentrations during pregnancy and children’s interpersonal, communication, repetitive, and stereotypic behaviors at 8 years of age: The home study. Environmental Research, 157, 9–16.CrossRefPubMedGoogle Scholar
  50. Mullen, B. R., Khialeeva, E., Hoffman, D. B., Ghiani, C. A., & Carpenter, E. M. (2012). Decreased reelin expression and organophosphate pesticide exposure alters mouse behaviour and brain morphology. ASN.Neuro, 5(1), e00106.PubMedPubMedCentralGoogle Scholar
  51. Mulligan, A., Richardson, T., Anney, R. J. L., & Gill, M. (2009). The Social Communication Questionnaire in a sample of the general population of school-going children. Irish Journal of Medical Science, 178(2), 193–199.CrossRefPubMedGoogle Scholar
  52. Pendyala, G., Chou, S., Jung, Y., Coiro, P., Spartz, E., Padmashri, R., et al. (2017). Maternal immune activation causes behavioral impairments and altered cerebellar cytokine and synaptic protein expression. Neuropsychopharmacology, 42(7), 1435–1446.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rahbar, M. H., Samms-Vaughan, M., Ardjomand-Hessabi, M., Loveland, K. A., Dickerson, A. S., Chen, Z., et al. (2012a). The role of drinking water sources, consumption of vegetables and seafood in relation to blood arsenic concentrations of Jamaican children with and without Autism Spectrum Disorders. Science of the Total Environment, 433, 362–370.CrossRefPubMedGoogle Scholar
  54. Rahbar, M. H., Samms-Vaughan, M., Loveland, K. A., Ardjomand-Hessabi, M., Chen, Z., Bressler, J., et al. (2013). Seafood consumption and blood mercury concentrations in Jamaican children with and without autism spectrum disorders. Neurotoxicity Research, 23(1), 22–38.CrossRefPubMedGoogle Scholar
  55. Rahbar, M. H., Samms-Vaughan, M., Loveland, K. A., Pearson, D. A., Bressler, J., Chen, Z., et al. (2012b). Maternal and paternal age are jointly associated with childhood autism in Jamaica. Journal of Autism and Developmental Disorders, 42(9), 1928–1938.CrossRefPubMedGoogle Scholar
  56. Roberson, S., Onugha, T., Siles, R. I., & Samms Vaughan, M. E. (2001). Obstetric complications and autism in Jamaican children. West Indian Med J, 50(Suppl 5), 13.Google Scholar
  57. Roberts, A. L., Lyall, K., Hart, J. E., Laden, F., Just, A. C., Bobb, J. F., et al. (2013). Perinatal air pollutant exposures and autism spectrum disorder in the children of Nurses’ Health Study II participants. Environmental Health Perspectives, 121(8), 978–984.PubMedPubMedCentralGoogle Scholar
  58. Roberts, E. M., English, P. B., Grether, J. K., Windham, G. C., Somberg, L., & Wolff, C. (2007). Maternal residence near agricultural pesticide applications and autism spectrum disorders among children in the California Central Valley. Environmental Health Perspectives, 115(10), 1482–1489. Scholar
  59. Rutter, M., Bailey, A., & Lord, C. (2003). SCQ: The social communication questionnaire-manual. Los Angeles, CA: Western Psychological Services.Google Scholar
  60. Rutter, M., LeCouteur, A., & Lord, C. (2003). Autism diagnostic interview, revised (ADI-R). Los Angeles, CA: Western Psychological Services.Google Scholar
  61. Samms-Vaughan, M. & Planning Institute of Jamaica.Policy Development Unit. (2000). Cognition, educational attainment, and behaviour in a cohort of Jamaican children: A comprehensive look at the development and behaviour of Jamaicas eleven year olds. Working paper (Planning Institute of Jamaica. Policy Development Unit) Policy Development Unit, Planning Institute of Jamaica.Google Scholar
  62. SAS Institute Inc. (2013). SAS® 9.4. Retrieved from SAS Institute Inc.Google Scholar
  63. Schmidt, R. J., Kogan, V., Shelton, J. F., Delwiche, L., Hansen, R. L., Ozonoff, S., et al. (2017). Combined Prenatal Pesticide Exposure and Folic Acid Intake in Relation to Autism Spectrum Disorder. Environmental Health Perspectives, 125(9), 097007. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Schopler, E., Reichler, R. J., DeVellis, R. F., & Daly, K. (1980). Toward objective classification of childhood autism: Childhood Autism Rating Scale (CARS). Journal of Autism and Developmental Disorders, 10(1), 91–103.CrossRefPubMedGoogle Scholar
  65. Schreibman, L. (1988). Diagnostic features of autism. Journal of Child Neurology, 3(1 suppl), S57–S64.Google Scholar
  66. Shelton, J. F., Geraghty, E. M., Tancredi, D. J., Delwiche, L. D., Schmidt, R. J., Ritz, B., et al. (2014). Neurodevelopmental disorders and prenatal residential proximity to agricultural pesticides: The CHARGE study. Environmental Health Perspectives, 122(10), 1103.Google Scholar
  67. Shelton, J. F., Hertz-Picciotto, I., & Pessah, I. N. (2012). Tipping the balance of autism risk: Potential mechanisms linking pesticides and autism. Environmental Health Perspectives, 120(7), 944–951. Scholar
  68. Shin, Y. Y., Park, A., Berrios, J., Lafourcade, M., Pascual, L. M., Soares, N., et al. (2017). Reversing behavioural abnormalities in mice exposed to maternal inflammation. Nature, 549(7673), 482–487.CrossRefGoogle Scholar
  69. Siles, R. I., & Samms Vaughan, M. E. (2001). Maternal stress associated with raising autistic children in Jamaica. West Indian Med.J, 50(Suppl 5), 26–27.Google Scholar
  70. Snead, M. C., Wiener, J., Ewumi, S., Phillips, C., Flowers, L., Hylton-Kong, T., et al. (2017). Prevalence and risk factors associated with STIs among women initiating contraceptive implants in Kingston, Jamaica. Sex Transmitted Infect, 93(7), 503–507.CrossRefGoogle Scholar
  71. Till, C., Koren, G., & Rovet, J. F. (2001). Prenatal exposure to organic solvents and child neurobehavioral performance. Neurotoxicology and Teratology, 23(3), 235–245.CrossRefPubMedGoogle Scholar
  72. Windham, G. C., Zhang, L., Gunier, R., Croen, L. A., & Grether, J. K. (2006). Autism spectrum disorders in relation to distribution of hazardous air pollutants in the san francisco bay area. Environmental Health Perspectives, 114(9), 1438–1444.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Wood, H., Drebot, M. A., Dewailly, E., Dillon, L., Dimitrova, K., Forde, M., et al. (2014). Seroprevalence of seven zoonotic pathogens in pregnant women from the Caribbean. American Journal of Tropical Medicine and Hygiene, 91(3), 642–644.CrossRefPubMedGoogle Scholar
  74. World Bank. (2010). Motor vehicles (per 1000 people). Retrieved from
  75. World Health Organization. (2017). Preterm birth [Fact sheet]. Retrieved from
  76. Xu, M., Sajdel-Sulkowska, E. M., Iwasaki, T., & Koibuchi, N. (2013). Aberrant cerebellar neurotrophin-3 expression induced by lipopolysaccharide exposure during brain development. Cerebellum, 12(3), 316–318.CrossRefPubMedGoogle Scholar
  77. Zerbo, O., Iosif, A. M., Walker, C., Ozonoff, S., Hansen, R. L., & Hertz-Picciotto, I. (2013). Is maternal influenza or fever during pregnancy associated with autism or developmental delays? Results from the CHARGE (CHildhood Autism Risks from Genetics and Environment) study. Journal of Autism and Developmental Disorders, 43(1), 25–33.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Zerbo, O., Qian, Y., Yoshida, C., Grether, J. K., Van de Water, J., & Croen, L. A. (2015). Maternal Infection During Pregnancy and Autism Spectrum Disorders. Journal of Autism and Developmental Disorders, 45(12), 4015–4025.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • MacKinsey A. Christian
    • 1
    • 2
  • Maureen Samms-Vaughan
    • 3
  • MinJae Lee
    • 2
    • 4
  • Jan Bressler
    • 5
  • Manouchehr Hessabi
    • 2
  • Megan L. Grove
    • 5
  • Sydonnie Shakespeare-Pellington
    • 3
  • Charlene Coore Desai
    • 3
  • Jody-Ann Reece
    • 3
  • Katherine A. Loveland
    • 6
  • Eric Boerwinkle
    • 5
    • 7
  • Mohammad H. Rahbar
    • 1
    • 2
    • 4
    Email author
  1. 1.Department of Epidemiology, Human Genetics, and Environmental SciencesSchool of Public Health, The University of Texas Health Science Center at HoustonHoustonUSA
  2. 2.Biostatistics/Epidemiology/Research Design (BERD) core, Center for Clinical and Translational Sciences (CCTS)The University of Texas Health Science Center at HoustonHoustonUSA
  3. 3.Department of Child and Adolescent HealthThe University of the West Indies (UWI)KingstonJamaica
  4. 4.Division of Clinical and Translational Sciences, Department of Internal MedicineThe University of Texas McGovern Medical SchoolHoustonUSA
  5. 5.Human Genetics Center, Department of Epidemiology, Human Genetics, and Environmental SciencesSchool of Public Health, The University of Texas Health Science Center at HoustonHoustonUSA
  6. 6.Department of Psychiatry and Behavioral SciencesThe University of Texas McGovern Medical SchoolHoustonUSA
  7. 7.Human Genome Sequencing CenterBaylor College of MedicineHoustonUSA

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