Skip to main content
Log in

Additive or Interactive Associations of Food Allergies with Glutathione S-Transferase Genes in Relation to ASD and ASD Severity in Jamaican Children

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

To investigate additive and interactive associations of food allergies with three glutathione S-transferase (GST) genes in relation to ASD and ASD severity in Jamaican children. Using data from 344 1:1 age- and sex-matched ASD cases and typically developing controls, we assessed additive and interactive associations of food allergies with polymorphisms in GST genes (GSTM1, GSTP1 and GSTT1) in relation to ASD by applying conditional logistic regression models, and in relation to ASD severity in ASD cases as measured by the Autism Diagnostic Observation Schedule-2nd Edition (ADOS-2) total and domains specific comparison scores (CSs) by fitting general linear models. Although food allergies and GST genes were not associated with ASD, ASD cases allergic to non-dairy food had higher mean ADOS-2 Restricted and Repetitive Behaviors (RRB) CS (8.8 vs. 8.0, P = 0.04). In addition, allergy to dairy was associated with higher mean RRB CS only among ASD cases with GSTT1 DD genotype (9.9 vs. 7.8, P < 0.01, interaction P = 0.01), and GSTP1 Val/Val genotype under a recessive genetic model (9.8 vs. 7.8, P = 0.02, interaction P = 0.06). Our findings are consistent with the role for GST genes in ASD and food allergies, though require replication in other populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alabdali, A., Al-Ayadhi, L., & El-Ansary, A. (2014). A key role for an impaired detoxification mechanism in the etiology and severity of autism spectrum disorders. Behavioral and Brain Functions. https://doi.org/10.1186/1744-9081-10-14

    Article  PubMed  PubMed Central  Google Scholar 

  • American Psychiatric Association. (2013). American Psychiatric Association: Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub.

    Book  Google Scholar 

  • Angelidou, A., Alysandratos, K. D., Asadi, S., Zhang, B., Francis, K., Vasiadi, M., Kalogeromitros, D., & Theoharides, T. C. (2011). Brief report: “allergic symptoms” in children with autism spectrum disorders. more than meets the eye? J Autism Developmental Disorder, 41(11), 1579–1585. https://doi.org/10.1007/s10803-010-1171-z

    Article  Google Scholar 

  • Bach, M. A., Samms-Vaughan, M., Hessabi, M., Bressler, J., Lee, M., Zhang, J., Shakespeare-Pellington, S., Grove, M. L., Loveland, K. A., & Rahbar, M. H. (2020). Association of polychlorinated biphenyls and organochlorine pesticides with autism spectrum disorder in Jamaican children. Research in Autism Spectrum Disorder, 76, 101587.

    Article  Google Scholar 

  • Barnes, K. C. (2010). Genomewide association studies in allergy and the influence of ethnicity. Current Opinion in Allergy and Clinical Immunology, 10(5), 427.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bavykina, I. A., Popov, V. I., Zvyagin, A. A., & Bavykin, D. V. (2019). Frequency of determining markers of casein’s inhability and gluten in children with disorders of autistic spectrum. Voprosy Pitaniia, 88(4), 41–47.

    PubMed  Google Scholar 

  • Berni Canani, R., Paparo, L., Nocerino, R., Di Scala, C., Della Gatta, G., Maddalena, Y., Buono, A., Bruno, C., Voto, L., & Ercolini, D. (2019). Gut Microbiome as target for innovative strategies against food allergy. Frontiers in Immunology, 10, 191. https://doi.org/10.3389/fimmu.2019.00191

    Article  PubMed  PubMed Central  Google Scholar 

  • Billeci, L., Tonacci, A., Tartarisco, G., Ruta, L., Pioggia, G., & Gangemi, S. (2016). Reply to fluegge: association between atopic dermatitis and autism spectrum disorders: a systematic review. American Journal of Clinical Dermatology, 17(2), 189–190. https://doi.org/10.1007/s40257-016-0181-9

    Article  PubMed  Google Scholar 

  • Bjørklund, G., & Chartrand, M. (2016). Nutritional and environmental influences on autism spectrum disorder. Journal Nutritions Disorders the, 6, e123.

    Google Scholar 

  • Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014). Microbiota and neurodevelopmental windows: Implications for brain disorders. Trends in Molecular Medicine, 20(9), 509–518. https://doi.org/10.1016/j.molmed.2014.05.002

    Article  PubMed  Google Scholar 

  • Bunyavanich, S., & Berin, M. C. (2019). Food allergy and the microbiome: Current understandings and future directions. Journal of Allergy and Clinical Immunology, 144(6), 1468–1477. https://doi.org/10.1016/j.jaci.2019.10.019

    Article  PubMed  Google Scholar 

  • Buratti, F. M., Darney, K., Vichi, S., Turco, L., Di Consiglio, E., Lautz, L. S., Béchaux, C., Dorne, J. C. M., & Testai, E. (2020). Human variability in glutathione-S-transferase activities, tissue distribution and major polymorphic variants: Meta-analysis and implication for chemical risk assessment. Toxicology Letters, 337, 78–90. https://doi.org/10.1016/j.toxlet.2020.11.007

    Article  PubMed  Google Scholar 

  • Carvalho, G., Moura, C. S., Roquetto, A. R., Barrera-Arellano, D., Yamada, A. T., Santos, A. D., Saad, M. J. A., & Amaya-Farfan, J. (2018). Impact of trans-fats on heat-shock protein expression and the gut microbiota profile of mice. Journal of Food Science, 83(2), 489–498. https://doi.org/10.1111/1750-3841.13997

    Article  PubMed  Google Scholar 

  • Castejon, A., & Spaw, J. (2014). Autism and oxidative stress interventions: Impact on autistic behavior. Austin Journal of Pharmacology and Therapeutics, 2(2), 1015.

    Google Scholar 

  • Cekici, H., & Sanlier, N. (2019). Current nutritional approaches in managing autism spectrum disorder: A review. Nutritional Neuroscience, 22(3), 145–155. https://doi.org/10.1080/1028415x.2017.1358481

    Article  PubMed  Google Scholar 

  • Chaidez, V., Hansen, R. L., & Hertz-Picciotto, I. (2014). Gastrointestinal problems in children with autism, developmental delays or typical development. Journal of Autism and Developmental Disorders, 44(5), 1117–1127.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cherevko, N., Skirnevskaya, A., Rosenstein, M. Y., Novikov, P., Muraveinik, O., & Denisov, A. (2018). Features of specific food hypersensitivity to dairy and cereal products in children with autism spectrum disorder. Bulletin of Siberian Medicine, 17(1), 159–166.

    Article  Google Scholar 

  • Chernikova, M. A., Flores, G. D., Kilroy, E., Labus, J. S., Mayer, E. A., & Aziz-Zadeh, L. (2021). The brain-gut-microbiome system: Pathways and implications for autism spectrum disorder. Nutrients. https://doi.org/10.3390/nu13124497

    Article  PubMed  PubMed Central  Google Scholar 

  • De Theije, C. G., Bavelaar, B. M., Lopes da Silva, S., Korte, S. M., Olivier, B., Garssen, J., & Kraneveld, A. D. (2014a). Food allergy and food-based therapies in neurodevelopmental disorders. Pediatric Allergy and Immunology, 25(3), 218–226.

    Article  PubMed  Google Scholar 

  • De Theije, C. G., Wu, J., Koelink, P. J., Korte-Bouws, G. A., Borre, Y., Kas, M. J., da Silva, S. L., Korte, S. M., Olivier, B., & Garssen, J. (2014b). Autistic-like behavioural and neurochemical changes in a mouse model of food allergy. Behavioural Brain Research, 261, 265–274.

    Article  PubMed  Google Scholar 

  • Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011). Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences, 108(7), 3047–3052. https://doi.org/10.1073/pnas.1010529108

    Article  Google Scholar 

  • Esler, A. N., Bal, V. H., Guthrie, W., Wetherby, A., Weismer, S. E., & Lord, C. (2015). The autism diagnostic observation schedule, toddler module: Standardized severity scores. Journal of Autism and Developmental Disorders, 45(9), 2704–2720.

    Article  PubMed  PubMed Central  Google Scholar 

  • Frustaci, A., Neri, M., Cesario, A., Adams, J. B., Domenici, E., Dalla Bernardina, B., & Bonassi, S. (2012). Oxidative stress-related biomarkers in autism: Systematic review and meta-analyses. Free Radical Biology and Medicine, 52(10), 2128–2141. https://doi.org/10.1016/j.freeradbiomed.2012.03.011

    Article  PubMed  Google Scholar 

  • Garrecht, M., & Austin, D. W. (2011). The plausibility of a role for mercury in the etiology of autism: A cellular perspective. Toxicological Environment Chemistry, 93(5–6), 1251–1273. https://doi.org/10.1080/02772248.2011.580588

    Article  Google Scholar 

  • Gilliland, F. D., Li, Y.-F., Saxon, A., & Diaz-Sanchez, D. (2004). Effect of glutathione-S-transferase M1 and P1 genotypes on xenobiotic enhancement of allergic responses: Randomised, placebo-controlled crossover study. The Lancet, 363(9403), 119–125.

    Article  Google Scholar 

  • Gotham, K., Pickles, A., & Lord, C. (2009). Standardizing ADOS scores for a measure of severity in autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(5), 693–705. https://doi.org/10.1007/s10803-008-0674-3

    Article  PubMed  Google Scholar 

  • Gupta, R. S., Warren, C. M., Smith, B. M., Blumenstock, J. A., Jiang, J., Davis, M. M., & Nadeau, K. C. (2018). The public health impact of parent-reported childhood food allergies in the United States. Pediatrics. https://doi.org/10.1542/peds.2018-1235

    Article  PubMed  PubMed Central  Google Scholar 

  • Gurney, J. G., McPheeters, M. L., & Davis, M. M. (2006). Parental report of health conditions and health care use among children with and without autism: National survey of children’s health. Archives of Pediatrics & Adolescent Medicine, 160(8), 825–830.

    Article  Google Scholar 

  • Hertz-Picciotto, I., Schmidt, R. J., & Krakowiak, P. (2018). Understanding environmental contributions to autism: Causal concepts and the state of science. Autism Research, 11(4), 554–586.

    Article  PubMed  Google Scholar 

  • Hus, V., Gotham, K., & Lord, C. (2014). Standardizing ADOS domain scores: Separating severity of social affect and restricted and repetitive behaviors. Journal of Autism and Developmental Disorders, 44(10), 2400–2412.

    Article  PubMed  PubMed Central  Google Scholar 

  • SAS Institute. (2013a). SAS/STAT® 13.1 User’s Guide: The GLM Procedure. https://support.sas.com/documentation/onlinedoc/stat/131/glm.pdf

  • SAS Institute. (2013b). SAS 9.4. In SAS Institute Inc Cary, NC.

  • Jackson, K. D., Howie, L. D., & Akinbami, L. J. (2013). Trends in allergic conditions among children: United States, 1997–2011. NCHS Data Brief, 121, 1–8.

    Google Scholar 

  • Jerónimo, C., Varzim, G., Henrique, R., Oliveira, J., Bento, M. J., Silva, C., Lopes, C., & Sidransky, D. (2002). I105V polymorphism and promoter methylation of the GSTP1 gene in prostate adenocarcinoma. Cancer Epidemiology Biomarkers Prevention, 11(5), 445–450.

    Google Scholar 

  • Jyonouchi, H., Geng, L., Cushing-Ruby, A., & Quraishi, H. (2008). Impact of innate immunity in a subset of children with autism spectrum disorders: A case control study. Journal Neuroinflammation, 5, 52. https://doi.org/10.1186/1742-2094-5-52

    Article  Google Scholar 

  • Kim, Y. H., Kim, K. W., Lee, S. Y., Koo, K. O., Kwon, S. O., Seo, J. H., Suh, D. I., Shin, Y. H., Ahn, K., Oh, S. Y., Lee, S., Sohn, M. H., & Hong, S. J. (2019). Maternal perinatal dietary patterns affect food allergy development in susceptible infants. Journal Allergy Clinical Immunology Practice, 7(7), 2337-2347.e2337. https://doi.org/10.1016/j.jaip.2019.03.026

    Article  Google Scholar 

  • Kim, Y. S., & Leventhal, B. L. (2015). Genetic epidemiology and insights into interactive genetic and environmental effects in autism spectrum disorders. Biological Psychiatry, 77(1), 66–74.

    Article  PubMed  Google Scholar 

  • Kleinbaum, D., & Klein, M. (2010). Logistic Regression: A Self-Learning Text, 3rd Springer Science+ Business Media. Springer.

    Book  Google Scholar 

  • König, J., Wells, J., Cani, P. D., García-Ródenas, C. L., MacDonald, T., Mercenier, A., Whyte, J., Troost, F., & Brummer, R. J. (2016). Human intestinal barrier function in health and disease. Clinical Translation Gastroenterology, 7(10), e196. https://doi.org/10.1038/ctg.2016.54

    Article  Google Scholar 

  • Lash, L. H., Chiu, W. A., Guyton, K. Z., & Rusyn, I. (2014). Trichloroethylene biotransformation and its role in mutagenicity, carcinogenicity and target organ toxicity. Mutation Research/reviews in Mutation Research, 762, 22–36.

    Article  PubMed  Google Scholar 

  • Lee, S. E., & Kim, H. (2016). Update on early nutrition and food allergy in children. Yonsei Medical Journal, 57(3), 542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, C., Liu, Y., Fang, H., Chen, Y., Weng, J., Zhai, M., Xiao, T., & Ke, X. (2020). Study on aberrant eating behaviors, food intolerance, and stereotyped behaviors in autism spectrum disorder. Front Psychiatry, 11, 493695. https://doi.org/10.3389/fpsyt.2020.493695

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, H., Liu, H., Chen, X., Zhang, J., Tong, G., & Sun, Y. (2021). Association of food hypersensitivity in children with the risk of autism spectrum disorder: A meta-analysis. European Journal of Pediatrics, 180(4), 999–1008. https://doi.org/10.1007/s00431-020-03826-x

    Article  PubMed  Google Scholar 

  • Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (1999). Autism diagnostic observation schedule-WPS (ADOS-WPS). Los Angeles: Western Psychological Services.

    Google Scholar 

  • Lucarelli, S., Frediani, T., Zingoni, A., Ferruzzi, F., Giardini, O., Quintieri, F., Barbato, M., D’eufemia, P., & Cardi, E. (1995). Food allergy and infantile autism. Panminerva Medica, 37(3), 137–141.

    PubMed  Google Scholar 

  • Ly, V., Bottelier, M., Hoekstra, P. J., Arias Vasquez, A., Buitelaar, J. K., & Rommelse, N. N. (2017). Elimination diets’ efficacy and mechanisms in attention deficit hyperactivity disorder and autism spectrum disorder. European Child and Adolescent Psychiatry, 26(9), 1067–1079. https://doi.org/10.1007/s00787-017-0959-1

    Article  PubMed  Google Scholar 

  • Lyall, K., Van de Water, J., Ashwood, P., & Hertz-Picciotto, I. (2015). Asthma and allergies in children with autism spectrum disorders: Results from the charge study. Autism Research, 8(5), 567–574. https://doi.org/10.1002/aur.1471

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma, J., Zhu, S. L., Liu, Y., Huang, X. Y., & Su, D. K. (2017). GSTP1 polymorphism predicts treatment outcome and toxicities for breast cancer. Oncotarget, 8(42), 72939–72949. https://doi.org/10.18632/oncotarget.18513

    Article  PubMed  PubMed Central  Google Scholar 

  • Mandic-Maravic, V., Pljesa-Ercegovac, M., Mitkovic-Voncina, M., Savic-Radojevic, A., Lecic-Tosevski, D., Simic, T., & Pejovic-Milovancevic, M. (2017). Impaired redox control in autism spectrum disorders: Could it be the x in gxe? Current Psychiatry Reports, 19(8), 52.

    Article  PubMed  Google Scholar 

  • Mandy, W., & Lai, M. C. (2016). Annual research review: The role of the environment in the developmental psychopathology of autism spectrum condition. Journal of Child Psychology and Psychiatry, 57(3), 271–292.

    Article  PubMed  Google Scholar 

  • Matelski, L., & Van de Water, J. (2016). Risk factors in autism: Thinking outside the brain. Journal of Autoimmunity, 67, 1–7. https://doi.org/10.1016/j.jaut.2015.11.003

    Article  PubMed  Google Scholar 

  • Menezo, Y. J., Elder, K., & Dale, B. (2015). Link between increased prevalence of autism spectrum disorder syndromes and oxidative stress, DNA methylation, and imprinting: The impact of the environment. JAMA Pediatrics, 169(11), 1066–1067. https://doi.org/10.1001/jamapediatrics.2015.2125

    Article  PubMed  Google Scholar 

  • Miyazaki, C., Koyama, M., Ota, E., Swa, T., Amiya, R. M., Mlunde, L. B., Tachibana, Y., Yamamoto-Hanada, K., & Mori, R. (2015). Allergies in children with autism spectrum disorder: A systematic review and meta-analysis. Review Journal of Autism and Developmental Disorders, 2(4), 374–401.

    Article  Google Scholar 

  • Moos, W. H., Faller, D. V., Harpp, D. N., Kanara, I., Pernokas, J., Powers, W. R., & Steliou, K. (2016). Microbiota and neurological disorders: A gut feeling. BioResearch Open Access, 5(1), 137–145.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mrozek-Budzyn, D., Majewska, R., Kiełyka, A., & Augustyniak, M. (2013). The frequency and risk factors of allergy and asthma in children with autism–case-control study. Przeglad Epidemiological, 67(4), 675–679.

    Google Scholar 

  • Neggers, Y. (2011). Dietary interventions in autism. In autism spectrum disorders – from genes to environment

  • Nemet, S., Asher, I., Yoles, I., Baevsky, T., & Sthoeger, Z. (2022). Early childhood allergy linked with development of attention deficit hyperactivity disorder and autism spectrum disorder. Pediatric Allergy and Immunology. https://doi.org/10.1111/pai.13819

    Article  PubMed  PubMed Central  Google Scholar 

  • Nigg, J. T., Lewis, K., Edinger, T., & Falk, M. (2012). Meta-analysis of attention-deficit/hyperactivity disorder or attention-deficit/hyperactivity disorder symptoms, restriction diet, and synthetic food color additives. Journal of the American Academy of Child & Adolescent Psychiatry, 51(1), 86-97.e88. https://doi.org/10.1016/j.jaac.2011.10.015

    Article  Google Scholar 

  • Pearce, N. (2016). Analysis of matched case-control studies. bmj, 352.

  • Pennesi, C. M., & Klein, L. C. (2012). Effectiveness of the gluten-free, casein-free diet for children diagnosed with autism spectrum disorder: Based on parental report. Nutritional Neuroscience, 15(2), 85–91. https://doi.org/10.1179/1476830512y.0000000003

    Article  PubMed  Google Scholar 

  • Peretti, S., Mariano, M., Mazzocchetti, C., Mazza, M., Pino, M. C., Verrotti Di Pianella, A., & Valenti, M. (2019). Diet: The keystone of autism spectrum disorder? Nutritional Neuroscience, 22(12), 825–839. https://doi.org/10.1080/1028415x.2018.1464819

    Article  PubMed  Google Scholar 

  • Perrier, C., & Corthésy, B. (2011). Gut permeability and food allergies. Clinical & Experimental Allergy, 41(1), 20–28. https://doi.org/10.1111/j.1365-2222.2010.03639.x

    Article  Google Scholar 

  • Piwowarczyk, A., Horvath, A., Łukasik, J., Pisula, E., & Szajewska, H. (2018). Gluten- and casein-free diet and autism spectrum disorders in children: A systematic review. European Journal of Nutrition, 57(2), 433–440. https://doi.org/10.1007/s00394-017-1483-2

    Article  PubMed  Google Scholar 

  • Portelli, M. A., Hodge, E., & Sayers, I. (2015). Genetic risk factors for the development of allergic disease identified by genome-wide association. Clinical & Experimental Allergy, 45(1), 21–31.

    Article  Google Scholar 

  • Posar, A., & Visconti, P. (2017). Autism in 2016: The need for answers. Jornal De Pediatria (versão Em Português), 93(2), 111–119.

    Article  Google Scholar 

  • Rachid, R., & Chatila, T. A. (2016). The role of the gut microbiota in food allergy. Current Opinion in Pediatrics, 28(6), 748–753. https://doi.org/10.1097/mop.0000000000000427

    Article  PubMed  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Ardjomand-Hessabi, M., Loveland, K. A., Dickerson, A. S., Chen, Z., Bressler, J., Shakespeare-Pellington, S., Grove, M. L., & Bloom, K. (2012). 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.

    Article  PubMed  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Lee, M., Zhang, J., Hessabi, M., Bressler, J., Bach, M. A., Grove, M. L., Shakespeare-Pellington, S., Beecher, C., McLaughlin, W., & Loveland, K. A. (2020). Interaction between a mixture of heavy metals (Lead, Mercury, Arsenic, Cadmium, Manganese, Aluminum) and GSTP1, GSTT1, and GSTM1 in relation to autism spectrum disorder. Research in Autism Spectrum Disorders. https://doi.org/10.1016/j.rasd.2020.101681

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Loveland, K. A., Ardjomand-Hessabi, M., Chen, Z., Bressler, J., Shakespeare-Pellington, S., Grove, M. L., Bloom, K., Pearson, D. A., Lalor, G. C., & Boerwinkle, E. (2013). Seafood consumption and blood mercury concentrations in jamaican children with and without autism spectrum disorders. Neurotoxicity Research, 23(1), 22–38. https://doi.org/10.1007/s12640-012-9321-z(NotinFile)

    Article  PubMed  Google Scholar 

  • Renzoni, E., Beltrami, V., Sestini, P., Pompella, A., Menchetti, G., & Zappella, M. (1995). Brief report: allergological evaluation of children with autism. Journal of Autism and Developmental Disorders, 25(3), 327–333. https://doi.org/10.1007/bf02179294

    Article  PubMed  Google Scholar 

  • Rogers, G. B., Keating, D. J., Young, R. L., Wong, M. L., Licinio, J., & Wesselingh, S. (2016). From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Molecular Psychiatry, 21(6), 738–748. https://doi.org/10.1038/mp.2016.50

    Article  PubMed  PubMed Central  Google Scholar 

  • Rutter, M., Bailey, A., & Lord, C. (2003). The social communication questionnaire: Manual. Western Psychological Services.

    Google Scholar 

  • Rutter, M., Le Couteur, A., & Lord, C. (2003). Autism diagnostic interview-revised. Los Angeles, CA: Western Psychological Services, 29, 30.

  • Saroukhani, S., Samms-Vaughan, M., Lee, M., Bach, M. A., Bressler, J., Hessabi, M., Grove, M. L., Shakespeare-Pellington, S., Loveland, K. A., & Rahbar, M. H. (2020). Perinatal factors associated with autism spectrum disorder in jamaican children. The Journal of Autism and Developmental Disorders, 50(9), 3341–3357. https://doi.org/10.1007/s10803-019-04229-0

    Article  PubMed  Google Scholar 

  • Schlosser, P. M., Bale, A. S., Gibbons, C. F., Wilkins, A., & Cooper, G. S. (2015). Human health effects of dichloromethane: Key findings and scientific issues. Environmental Health Perspectives, 123(2), 114–119.

    Article  PubMed  Google Scholar 

  • Sivamaruthi, B. S., Suganthy, N., Kesika, P., & Chaiyasut, C. (2020). The role of microbiome, dietary supplements, and probiotics in autism spectrum disorder. International Journal of Environmental Research and Public Health. https://doi.org/10.3390/ijerph17082647

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith, N. A., Germundson, D. L., Gao, P., Hur, J., Floden, A. M., & Nagamoto-Combs, K. (2021). Anxiety-like behavior and intestinal microbiota changes as strain-and sex-dependent sequelae of mild food allergy in mouse models of cow’s milk allergy. Brain, Behavior, and Immunity, 95, 122–141. https://doi.org/10.1016/j.bbi.2021.03.002

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan, T. T., Ellis, J., Saffery, R., & Allen, K. (2012). The role of genetics and environment in the rise of childhood food allergy. Clinical & Experimental Allergy, 42(1), 20–29.

    Article  Google Scholar 

  • Tan, Y., Thomas, S., & Lee, B. K. (2019). Parent-reported prevalence of food allergies in children with autism spectrum disorder: National health interview survey. Autism Research, 12(5), 802–805. https://doi.org/10.1002/aur.2106

    Article  PubMed  Google Scholar 

  • Tham, E. H., & Leung, D. Y. (2018). How different parts of the world provide new insights into food allergy. Allergy, Asthma & Immunology Research, 10(4), 290.

    Article  Google Scholar 

  • Wang, Y., & Kasper, L. H. (2014). The role of microbiome in central nervous system disorders. Brain, Behavior, and Immunity, 38, 1–12. https://doi.org/10.1016/j.bbi.2013.12.015

    Article  PubMed  Google Scholar 

  • Whiteley, P., Haracopos, D., Knivsberg, A.-M., Reichelt, K. L., Parlar, S., Jacobsen, J., Seim, A., Pedersen, L., Schondel, M., & Shattock, P. (2010). The ScanBrit randomised, controlled, single-blind study of a gluten-and casein-free dietary intervention for children with autism spectrum disorders. Nutritional Neuroscience, 13(2), 87–100.

    Article  PubMed  Google Scholar 

  • Xu, G., Snetselaar, L. G., Jing, J., Liu, B., Strathearn, L., & Bao, W. (2018). Association of food allergy and other allergic conditions with autism spectrum disorder in children. JAMA Network Open, 1(2), e180279. https://doi.org/10.1001/jamanetworkopen.2018.0279

    Article  PubMed  PubMed Central  Google Scholar 

  • Yadama, A. P., Kelly, R. S., Lee-Sarwar, K., Mirzakhani, H., Chu, S. H., Kachroo, P., Litonjua, A. A., Lasky-Su, J., & Weiss, S. T. (2020). Allergic disease and low ASQ communication score in children. Brain, Behavior, and Immunity, 83, 293–297. https://doi.org/10.1016/j.bbi.2019.10.008

    Article  PubMed  Google Scholar 

  • Zerbo, O., Leong, A., Barcellos, L., Bernal, P., Fireman, B., & Croen, L. A. (2015). Immune mediated conditions in autism spectrum disorders. Brain, Behavior, and Immunity, 46, 232–236. https://doi.org/10.1016/j.bbi.2015.02.001

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, Z.-J., Hao, K., Shi, R., Zhao, G., Jiang, G.-X., Song, Y., Xu, X., & Ma, J. (2011). Glutathione S-transferase M1 (GSTM1) and glutathione S-transferase T1 (GSTT1) null polymorphisms, smoking, and their interaction in oral cancer: A HuGE review and meta-analysis. American Journal of Epidemiology, 173(8), 847–857.

    Article  PubMed  Google Scholar 

  • Zhou, L., Chen, L., Li, X., Li, T., Dong, Z., & Wang, Y. T. (2019). Food allergy induces alteration in brain inflammatory status and cognitive impairments. Behavioural Brain Research, 364, 374–382. https://doi.org/10.1016/j.bbr.2018.01.011

    Article  PubMed  Google Scholar 

  • Zhou, T.-B., Drummen, G. P., Jiang, Z.-P., & Qin, Y.-H. (2014). GSTT1 polymorphism and the risk of developing prostate cancer. American Journal of Epidemiology, 180(1), 1–10.

    Article  PubMed  Google Scholar 

Download references

Funding

This research is funded by the National Institute of Environmental Health Sciences (NIEHS) by a grant (R01ES022165), as well as 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) awarded to 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 University of Texas Health Science Center at Houston in 2006 by the National Center for Research Resources (NCRR), and its 2012 renewal (UL1 TR000371) as well as another 2019 grant (UL1TR003167) by the National Center for Advancing Translational Sciences (NCATS). Furthermore, we acknowledge that the data management was done using REDCap (Harris et al. 2009). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIEHS, NICHD, NIH-FIC, NCRR, or NCATS.

Author information

Authors and Affiliations

Authors

Contributions

SS was primarily responsible for conceptualization, analyzing the data, interpreting the findings, and drafting the manuscript. MHR is the 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 SS’s PhD Epidemiology dissertation 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. JB and KL are co-Investigators of the ERAJ and ERAJ-2 studies who contributed to the study design, and also served on SS’s PhD Epidemiology dissertation committee and participated in revising the manuscript. ML and CBW served on SS’s PhD Epidemiology dissertation committee and participated in interpreting the findings and revising the manuscript. MH is responsible for data management of the ERAJ and ERAJ-2 studies and participated in revising the manuscript. MLG participated in revising the manuscript. SSP was responsible for data collection and participated in revising the manuscript. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Mohammad H. Rahbar.

Ethics declarations

Conflict of interest

All the authors declares that he has no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saroukhani, S., Samms-Vaughan, M., Bressler, J. et al. Additive or Interactive Associations of Food Allergies with Glutathione S-Transferase Genes in Relation to ASD and ASD Severity in Jamaican Children. J Autism Dev Disord 54, 704–724 (2024). https://doi.org/10.1007/s10803-022-05813-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-022-05813-7

Keywords

Navigation