Skip to main content
Log in

Interaction of Blood Manganese Concentrations with GSTT1 in Relation to Autism Spectrum Disorder in Jamaican Children

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

Abstract

Using data from 266 age- and sex-matched pairs of Jamaican children with autism spectrum disorder (ASD) and typically developing (TD) controls (2–8 years), we investigated whether glutathione S-transferase theta 1 (GSTT1) modifies the association between blood manganese concentrations (BMC) and ASD. After adjusting conditional logistic regression models for socioeconomic status and the interaction between GSTT1 and GSTP1 (glutathione S-transferase pi 1), using a recessive genetic model for GSTT1 and either a co-dominant or dominant model for GSTP1, the interaction between GSTT1 and BMC was significant (P = 0.02, P = 0.01, respectively). Compared to controls, ASD cases with GSTT1-DD genotype had 4.33 and 4.34 times higher odds of BMC > 12 vs. ≤ 8.3 μg/L, respectively. Replication in other populations is warranted.

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

  • Agency for Toxic Substances and Disease Registry (ATSDR). (2012a). Public health statement - manganese. https://www.atsdr.cdc.gov/ToxProfiles/tp151-c1-b.pdf. Accessed 05 June 2020.

  • Agency for Toxic Substances and Disease Registry (ATSDR). (2012b). Toxicological profile for manganese. https://www.atsdr.cdc.gov/ToxProfiles/tp151.pdf. Accessed 05 June 2020.

  • Abdullah, M. M., Ly, A. R., Goldberg, W. A., Clarke-Stewart, K. A., Dudgeon, J. V., Mull, C. G., et al. (2012). Heavy metal in children's tooth enamel: related to autism and disruptive behaviors? Journal of Autism and Developmental Disorders, 42(6), 929–936. https://doi.org/10.1007/s10803-011-1318-6.

    Article  PubMed  Google Scholar 

  • Adams, J. B., Holloway, C. E., George, F., & Quig, D. (2006). Analyses of toxic metals and essential minerals in the hair of Arizona children with autism and associated conditions, and their mothers. Biological Trace Element Research, 110(3), 193–209. https://doi.org/10.1385/bter:110:3:193.

    Article  PubMed  Google Scholar 

  • Al-Ayadhi, L. Y. (2005). Heavy metals and trace elements in hair samples of autistic children in central Saudi Arabia. Neurosciences (Riyadh), 10(3), 213–218.

    Google Scholar 

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

  • Aynacioglu, A. S., Nacak, M., Filiz, A., Ekinci, E., & Roots, I. (2004). Protective role of glutathione S-transferase P1 (GSTP1) Val105Val genotype in patients with bronchial asthma. British Journal of Clinical Pharmacology, 57(2), 213–217. https://doi.org/10.1046/j.1365-2125.2003.01975.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhang, S. Y., Cho, S. C., Kim, J. W., Hong, Y. C., Shin, M. S., Yoo, H. J., et al. (2013). Relationship between blood manganese levels and children's attention, cognition, behavior, and academic performance–a nationwide cross-sectional study. Environmental Research, 126, 9–16. https://doi.org/10.1016/j.envres.2013.05.006.

    Article  PubMed  Google Scholar 

  • Bjørklund, G., Meguid, N.A., El-Bana, M.A., Tinkov, A.A., Saad, K., Dadar, M., et al. (2020). Oxidative stress in autism spectrum disorder. Molecular Neurobiology, 1–19.

  • Blaurock-Busch, E., Amin, O. R., & Rabah, T. (2011). Heavy metals and trace elements in hair and urine of a sample of arab children with autistic spectrum disorder. Maedica (Buchar), 6(4), 247–257.

    Google Scholar 

  • Bouchard, M. F., Sauve, S., Barbeau, B., Legrand, M., Brodeur, M. E., Bouffard, T., et al. (2011). Intellectual impairment in school-age children exposed to manganese from drinking water. Environmental Health Perspectives, 119(1), 138–143. https://doi.org/10.1289/ehp.1002321.

    Article  PubMed  Google Scholar 

  • Cai, Q., Wang, Z., Zhang, W., Guo, X., Shang, Z., Jiang, N., et al. (2014). Association between glutathione S-transferases M1 and T1 gene polymorphisms and prostate cancer risk: a systematic review and meta-analysis. Tumor Biology, 35(1), 247–256.

    Article  Google Scholar 

  • Carvalho, C. F., Menezes-Filho, J. A., de Matos, V. P., Bessa, J. R., Coelho-Santos, J., Viana, G. F., et al. (2014). Elevated airborne manganese and low executive function in school-aged children in Brazil. Neurotoxicology, 45, 301–308.

    Article  Google Scholar 

  • Chiu, Y. M., Claus Henn, B., Hsu, H. L., Pendo, M. P., Coull, B. A., Austin, C., et al. (2017). Sex differences in sensitivity to prenatal and early childhood manganese exposure on neuromotor function in adolescents. Environmental Research, 159, 458–465. https://doi.org/10.1016/j.envres.2017.08.035.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chung, S. E., Cheong, H.-K., Ha, E.-H., Kim, B.-N., Ha, M., Kim, Y., et al. (2015). Maternal blood manganese and early neurodevelopment: the mothers and children’s environmental health (MOCEH) study. Environmental health perspectives, 123(7), 717–722.

    Article  Google Scholar 

  • Claus Henn, B., Ettinger, A. S., Schwartz, J., Tellez-Rojo, M. M., Lamadrid-Figueroa, H., Hernandez-Avila, M., et al. (2010). Early postnatal blood manganese levels and children's neurodevelopment. Epidemiology, 21(4), 433–439. https://doi.org/10.1097/ede.0b013e3181df8e52.

    Article  PubMed  Google Scholar 

  • De Palma, G., Catalani, S., Franco, A., Brighenti, M., & Apostoli, P. (2012). Lack of correlation between metallic elements analyzed in hair by ICP-MS and autism. Journal of Autism and Developmental Disorders, 42(3), 342–353. https://doi.org/10.1007/s10803-011-1245-6.

    Article  PubMed  Google Scholar 

  • de Water, E., Papazaharias, D. M., Ambrosi, C., Mascaro, L., Iannilli, E., Gasparotti, R., et al. (2019). Early-life dentine manganese concentrations and intrinsic functional brain connectivity in adolescents: A pilot study. PLoS ONE, 14(8), e0220790. https://doi.org/10.1371/journal.pone.0220790.

    Article  PubMed  PubMed Central  Google Scholar 

  • Diedrich, A., Bock, H., König, F., Schulz, T., Ludwig, H., Herken, R., et al. (2006). Expression of glutathione S-transferase T1 GSTT1 in human brain tumours. Histology and histopathology.

  • Elsabbagh, M., Divan, G., Koh, Y. J., Kim, Y. S., Kauchali, S., Marcín, C., et al. (2012). Global prevalence of autism and other pervasive developmental disorders. Autism Research, 5(3), 160–179.

    Article  Google Scholar 

  • Environmental Protection Agency (EPA). (2007). Manganese toxicity and exposure assessment for children's health (TEACH) chemical summary. https://archive.epa.gov/region5/teach/web/pdf/manganese_summary.pdf. Accessed 05 June 2020.

  • Ercegovac, M., Jovic, N., Sokic, D., Savic-Radojevic, A., Coric, V., Radic, T., et al. (2015). GSTA1, GSTM1, GSTP1 and GSTT1 polymorphisms in progressive myoclonus epilepsy: A Serbian case–control study. Seizure, 32, 30–36.

    Article  Google Scholar 

  • Ericson, J. E., Crinella, F. M., Clarke-Stewart, K. A., Allhusen, V. D., Chan, T., & Robertson, R. T. (2007). Prenatal manganese levels linked to childhood behavioral disinhibition. Neurotoxicology and Teratology, 29(2), 181–187. https://doi.org/10.1016/j.ntt.2006.09.020.

    Article  PubMed  Google Scholar 

  • Erikson, K. M., Dobson, A. W., Dorman, D. C., & Aschner, M. (2004). Manganese exposure and induced oxidative stress in the rat brain. Science of the Total Environment, 334–335, 409–416. https://doi.org/10.1016/j.scitotenv.2004.04.044.

    Article  Google Scholar 

  • Fernsebner, K., Zorn, J., Kanawati, B., Walker, A., & Michalke, B. (2014). Manganese leads to an increase in markers of oxidative stress as well as to a shift in the ratio of Fe(II)/(III) in rat brain tissue. Metallomics, 6(4), 921–931. https://doi.org/10.1039/c4mt00022f.

    Article  PubMed  Google Scholar 

  • Frustaci, A., Neri, M., Cesario, A., Adams, J. B., Domenici, E., Dalla Bernardina, B., et al. (2012). Oxidative stress-related biomarkers in autism: systematic review and meta-analyses. Free Radic Biol Med, 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 and Environmental Chemistry, 93(5–6), 1251–1273. https://doi.org/10.1080/02772248.2011.580588.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gavin, C. E., Gunter, K. K., & Gunter, T. E. (1990). Manganese and calcium efflux kinetics in brain mitochondria. Relevance to manganese toxicity. Biochemical Journal, 266(2), 329–334. https://doi.org/10.1042/bj2660329.

    Article  PubMed Central  Google Scholar 

  • Gavin, C. E., Gunter, K. K., & Gunter, T. E. (1999). Manganese and calcium transport in mitochondria: Implications for manganese toxicity. Neurotoxicology, 20(2–3), 445–453.

    PubMed  Google Scholar 

  • Giulivi, C., Zhang, Y. F., Omanska-Klusek, A., Ross-Inta, C., Wong, S., Hertz-Picciotto, I., et al. (2010). Mitochondrial dysfunction in autism. Jama, 304(21), 2389–2396. https://doi.org/10.1001/jama.2010.1706.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guan, H., Wang, M., Li, X., Piao, F., Li, Q., Xu, L., et al. (2014). Manganese concentrations in maternal and umbilical cord blood: Related to birth size and environmental factors. The European Journal of Public Health, 24(1), 150–157.

    Article  Google Scholar 

  • Hallmayer, J., Cleveland, S., Torres, A., Phillips, J., Cohen, B., Torigoe, T., et al. (2011). Genetic heritability and shared environmental factors among twin pairs with autism. Archives of General Psychiatry, 68(11), 1095–1102.

    Article  Google Scholar 

  • Harris, P. A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N., & Conde, J. G. (2009). Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. Journal of Biomedical Informatics, 42(2), 377–381.

    Article  Google Scholar 

  • Hayes, J. D., & Strange, R. C. (2000). Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology, 61(3), 154–166.

    Article  Google Scholar 

  • Haynes, E. N., Sucharew, H., Kuhnell, P., Alden, J., Barnas, M., Wright, R. O., et al. (2015). Manganese exposure and neurocognitive outcomes in rural school-age children: The communities actively researching exposure study (Ohio, USA). Environmental health perspectives, 123(10), 1066–1071.

    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  Google Scholar 

  • Hong, S.-B., Kim, J.-W., Choi, B.-S., Hong, Y.-C., Park, E.-J., Shin, M.-S., et al. (2014). Blood manganese levels in relation to comorbid behavioral and emotional problems in children with attention-deficit/hyperactivity disorder. Psychiatry Research, 220(1–2), 418–425.

    Article  Google Scholar 

  • Hope, S., Daniel, K., Gleason, K. L., Comber, S., Nelson, M., & Powell, J. J. (2006). Influence of tea drinking on manganese intake, manganese status and leucocyte expression of MnSOD and cytosolic aminopeptidase P. European Journal of Clinical Nutrition, 60(1), 1–8. https://doi.org/10.1038/sj.ejcn.1602260.

    Article  PubMed  Google Scholar 

  • Howe, A., Fung, L. H., Lalor, G., Rattray, R., & Vutchkov, M. (2005). Elemental composition of Jamaican foods 1: A survey of five food crop categories. Environmental Geochemistry and Health, 27(1), 19–30. https://doi.org/10.1007/s10653-004-5671-7.

    Article  PubMed  Google Scholar 

  • James, S. J., Melnyk, S., Jernigan, S., Cleves, M. A., Halsted, C. H., Wong, D. H., et al. (2006). Metabolic endophenotype and related genotypes are associated with oxidative stress in children with autism. American Journal of Medical Genetics, 141(8), 947–956. https://doi.org/10.1002/ajmg.b.30366.

    Article  Google Scholar 

  • Janka, Z. (2019). Tracing trace elements in mental functions. Ideggyogyaszati Szemle, 72(11–12), 367.

    Article  Google Scholar 

  • Jory, J., & McGinnis, W. R. (2008). Red-cell trace minerals in children with autism. American Journal of Biochemistry and Biotechnology, 4(2), 101–104.

    Article  Google Scholar 

  • Khan, K., Factor-Litvak, P., Wasserman, G. A., Liu, X., Ahmed, E., Parvez, F., et al. (2011). Manganese exposure from drinking water and children's classroom behavior in Bangladesh. Environmental Health Perspectives, 119(10), 1501–1506. https://doi.org/10.1289/ehp.1003397.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan, K., Wasserman, G. A., Liu, X., Ahmed, E., Parvez, F., Slavkovich, V., et al. (2012). Manganese exposure from drinking water and children's academic achievement. Neurotoxicology, 33(1), 91–97. https://doi.org/10.1016/j.neuro.2011.12.002.

    Article  PubMed  Google Scholar 

  • Kim, Y., Kim, B. N., Hong, Y. C., Shin, M. S., Yoo, H. J., Kim, J. W., et al. (2009). Co-exposure to environmental lead and manganese affects the intelligence of school-aged children. Neurotoxicology, 30(4), 564–571. https://doi.org/10.1016/j.neuro.2009.03.012.

    Article  PubMed  Google Scholar 

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

  • Koh, E. S., Kim, S. J., Yoon, H. E., Chung, J. H., Chung, S., Park, C. W., et al. (2014). Association of blood manganese level with diabetes and renal dysfunction: a cross-sectional study of the Korean general population. BMC Endocr Disord, 14, 24. https://doi.org/10.1186/1472-6823-14-24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lalor, G. C. (1996). Geochemical mapping in Jamaica. Environmental Geochemistry and Health, 18(3), 89–97. https://doi.org/10.1007/bf01771284.

    Article  PubMed  Google Scholar 

  • Landi, S. (2000). Mammalian class theta GST and differential susceptibility to carcinogens: A review. Mutation Research/Reviews in Mutation Research, 463(3), 247–283.

    Article  Google Scholar 

  • Landrigan, P. J., Lambertini, L., & Birnbaum, L. S. (2012). A research strategy to discover the environmental causes of autism and neurodevelopmental disabilities. Environmental Health Perspectives, 120(7), a258–260. https://doi.org/10.1289/ehp.1104285.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee, J.-Y., Hwang, I.-W., Lim, M.-H., Kwon, H.-J., & Jin, H.-J. (2016). Association of glutathione S-transferases M1, T1 and P1 gene polymorphisms with attention deficit and hyperactivity disorder in Korean children. Gene, 586(2), 228–233.

    Article  Google Scholar 

  • Lin, C.-C., Chen, Y.-C., Su, F.-C., Lin, C.-M., Liao, H.-F., Hwang, Y.-H., et al. (2013). In utero exposure to environmental lead and manganese and neurodevelopment at 2 years of age. Environmental research, 123, 52–57.

    Article  Google Scholar 

  • Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., Bishop, S., et al. (2015). ADOS-2. Escala de Observación para el Diagnóstico del Autismo-2. Manual (T. Luque, adaptadora). Madrid: TEA Ediciones.

  • Lucchini, R., Placidi, D., Cagna, G., Fedrighi, C., Oppini, M., Peli, M., et al. (2017). Manganese and developmental neurotoxicity. In: Neurotoxicity of Metals (pp. 13–34): Springer.

  • Mandic-Maravic, V., Coric, V., Mitkovic-Voncina, M., Djordjevic, M., Savic-Radojevic, A., Ercegovac, M., et al. (2019). Interaction of glutathione S-transferase polymorphisms and tobacco smoking during pregnancy in susceptibility to autism spectrum disorders. Scientific Reports, 9(1), 1–9.

    Article  Google Scholar 

  • Matelski, L., & Van de Water, J. (2016). Risk factors in autism: Thinking outside the brain. Journal of autoimmunity, 67, 1–7.

    Article  Google Scholar 

  • Menezes-Filho, J. A., de Carvalho-Vivas, C. F., Viana, G. F., Ferreira, J. R., Nunes, L. S., Mergler, D., et al. (2014). Elevated manganese exposure and school-aged children's behavior: A gender-stratified analysis. Neurotoxicology, 45, 293–300.

    Article  Google Scholar 

  • Menezes-Filho, J. A., Novaes Cde, O., Moreira, J. C., Sarcinelli, P. N., & Mergler, D. (2011). Elevated manganese and cognitive performance in school-aged children and their mothers. Environmental Research, 111(1), 156–163. https://doi.org/10.1016/j.envres.2010.09.006.

    Article  PubMed  Google Scholar 

  • Mora, A. M., Arora, M., Harley, K. G., Kogut, K., Parra, K., Hernández-Bonilla, D., et al. (2015). Prenatal and postnatal manganese teeth levels and neurodevelopment at 7, 9, and 10.5 years in the CHAMACOS cohort. Environment International, 84, 39–54. https://doi.org/10.1016/j.envint.2015.07.009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Neal, A. P., & Guilarte, T. R. (2013). Mechanisms of lead and manganese neurotoxicity. Toxicology research, 2(2), 99–114.

    Article  Google Scholar 

  • Nebert, D. W., & Vasiliou, V. (2004). Analysis of the glutathione S-transferase (GST) gene family. Hum Genomics, 1(6), 460–464. https://doi.org/10.1186/1479-7364-1-6-460.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pagano, G., Talamanca, A. A., Castello, G., Cordero, M. D., d'Ischia, M., Gadaleta, M. N., et al. (2014). Oxidative stress and mitochondrial dysfunction across broad-ranging pathologies: Toward mitochondria-targeted clinical strategies. Oxid Med Cell Longev, 2014, 541230. https://doi.org/10.1155/2014/541230.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Dickerson, A. S., Loveland, K. A., Ardjomand-Hessabi, M., Bressler, J., et al. (2014). Blood manganese concentrations in Jamaican children with and without autism spectrum disorders. Environmental Health, 13(1), 69–82.

    Article  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Lee, M., Christian, M. A., Bressler, J., Hessabi, M., et al. (2018). Interaction between manganese and GSTP1 in relation to autism spectrum disorder while controlling for exposure to mixture of lead, mercury, arsenic, and cadmium. Research in Autism Spectrum Disorders, 55, 50–63. https://doi.org/10.1016/j.rasd.2018.08.003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Ma, J., Bressler, J., Dickerson, A. S., Hessabi, M., et al. (2015a). Synergic effect of GSTP1 and blood manganese concentrations in autism spectrum disorder. Research in Autism Spectrum Disorders, 18(10), 73–82.

    Article  Google Scholar 

  • Rahbar, M. H., Samms-Vaughan, M., Ma, J., Bressler, J., Loveland, K. A., Hessabi, M., et al. (2015b). Interaction between GSTT1 and GSTP1 allele variants as a risk modulating-factor for autism spectrum disorders. Research in Autism Spectrum Disorders, 12, 1–9. https://doi.org/10.1016/j.rasd.2014.12.008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahman, S. M., Kippler, M., Tofail, F., Bölte, S., Derakhshani Hamadani, J., & Vahter, M. (2017). Manganese in drinking water and cognitive abilities and behavior at 10 years of age: A prospective cohort study. Environmental Health Perspectives, 125(5), 057003.

    Article  Google Scholar 

  • Ritambhara, Tiwari, S., Vijayaraghavalu, S., & Kumar, M. (2019). Genetic polymorphisms of xenobiotic metabolizing genes (GSTM1, GSTT1, GSTP1), gene-gene interaction with association to lung cancer risk in north india; a case control study. Asian Pacific Journal of Cancer Prevention, 20(9), 2707–2714.

    Article  Google Scholar 

  • Roels, H. A., Bowler, R. M., Kim, Y., Claus Henn, B., Mergler, D., Hoet, P., et al. (2012). Manganese exposure and cognitive deficits: A growing concern for manganese neurotoxicity. Neurotoxicology, 33(4), 872–880. https://doi.org/10.1016/j.neuro.2012.03.009.

    Article  PubMed  Google Scholar 

  • Rossignol, D. A., Genuis, S. J., & Frye, R. E. (2014). Environmental toxicants and autism spectrum disorders: A systematic review. Translational psychiatry, 4(2), e360–e360.

    Article  Google Scholar 

  • Rucker, D., Thadhani, R., & Tonelli, M. (2010). Trace element status in hemodialysis patients. Seminars in Dialysis, 23(4), 389–395. https://doi.org/10.1111/j.1525-139X.2010.00746.x.

    Article  PubMed  Google Scholar 

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

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

    Google Scholar 

  • SAS Institute. (2013). SAS 9.4 online documentation. SAS Institute Inc Cary, NC.

  • Schieve, L. A., Tian, L. H., Drews-Botsch, C., Windham, G. C., Newschaffer, C., Daniels, J. L., et al. (2018). Autism spectrum disorder and birth spacing: Findings from the study to explore early development (SEED). Autism Research, 11(1), 81–94.

    Article  Google Scholar 

  • Schmidt, R. J., Hansen, R. L., Hartiala, J., Allayee, H., Schmidt, L. C., Tancredi, D. J., et al. (2011). Prenatal vitamins, one-carbon metabolism gene variants, and risk for autism. Epidemiology, 22(4), 476–485. https://doi.org/10.1097/EDE.0b013e31821d0e30.

    Article  PubMed  PubMed Central  Google Scholar 

  • St-Pierre, A., Normandin, L., Carrier, G., Kennedy, G., Butterworth, R., & Zayed, J. (2001). Bioaccumulation and locomotor effect of manganese dust in rats. Inhal Toxicol, 13(7), 623–632. https://doi.org/10.1080/08958370117066.

    Article  PubMed  Google Scholar 

  • Taioli, E., Flores-Obando, R. E., Agalliu, I., Blanchet, P., Bunker, C. H., Ferrell, R. E., et al. (2011). Multi-institutional prostate cancer study of genetic susceptibility in populations of African descent. Carcinogenesis, 32(9), 1361–1365. https://doi.org/10.1093/carcin/bgr119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Takser, L., Mergler, D., Hellier, G., Sahuquillo, J., & Huel, G. (2003). Manganese, monoamine metabolite levels at birth, and child psychomotor development. Neurotoxicology, 24(4–5), 667–674. https://doi.org/10.1016/s0161-813x(03)00058-5.

    Article  PubMed  Google Scholar 

  • Tamai, T., Uto, H., Takami, Y., Oda, K., Saishoji, A., Hashiguchi, M., et al. (2011). Serum manganese superoxide dismutase and thioredoxin are potential prognostic markers for hepatitis C virus-related hepatocellular carcinoma. World Journal of Gastroenterology, 17(44), 4890–4898. https://doi.org/10.3748/wjg.v17.i44.4890.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang, K., Xue, W., Xing, Y., Xu, S., Wu, Q., Liu, R., et al. (2012). Genetic polymorphisms of glutathione S-Transferase M1, T1, and P1, and the assessment of oxidative damage in infertile men with varicoceles from northwestern China. Journal of andrology, 33(2), 257–263.

    Article  Google Scholar 

  • Vojtková, J., Ďurdík, P., Čiljaková, M., Michnová, Z., Turčan, T., & Babušíková, E. (2013). The association between gene polymorphisms of glutathione S-transferase T1/M1 and type 1 diabetes in Slovak children and adolescents. Central European Journal of Public Health, 21(2), 88–91.

    Article  Google Scholar 

  • Wasserman, G. A., Liu, X., Parvez, F., Factor-Litvak, P., Ahsan, H., Levy, D., et al. (2011). Arsenic and manganese exposure and children's intellectual function. Neurotoxicology, 32(4), 450–457. https://doi.org/10.1016/j.neuro.2011.03.009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams, T. A., Mars, A. E., Buyske, S. G., Stenroos, E. S., Wang, R., Factura-Santiago, M. F., et al. (2007). Risk of autistic disorder in affected offspring of mothers with a glutathione S-transferase P1 haplotype. Archives of Pediatrics and Adolescent Medicine, 161(4), 356–361. https://doi.org/10.1001/archpedi.161.4.356.

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1289/ehp.9120.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright, R. O., Amarasiriwardena, C., Woolf, A. D., Jim, R., & Bellinger, D. C. (2006). Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology, 27(2), 210–216. https://doi.org/10.1016/j.neuro.2005.10.001.

    Article  PubMed  Google Scholar 

  • Wu, H. J., Seib, K. L., Srikhanta, Y. N., Edwards, J., Kidd, S. P., Maguire, T. L., et al. (2010). Manganese regulation of virulence factors and oxidative stress resistance in Neisseria gonorrhoeae. Journal of Proteomics, 73(5), 899–916. https://doi.org/10.1016/j.jprot.2009.12.001.

    Article  PubMed  Google Scholar 

  • Yuan, L., Ma, W., Liu, J., Meng, L., Liu, J., Li, S., et al. (2014). Effects of GSTM1/GSTT1 gene polymorphism and fruit & vegetable consumption on antioxidant biomarkers and cognitive function in the elderly: a community based cross-sectional study. PloS one, 9(11).

  • Yuan, L., Zhang, L., Ma, W., Zhou, X., Ji, J., Li, N., et al. (2013). Glutathione S-transferase M1 and T1 gene polymorphisms with consumption of high fruit-juice and vegetable diet affect antioxidant capacity in healthy adults. Nutrition, 29(7–8), 965–971.

    Article  Google Scholar 

  • Zhang, Z.-J., Hao, K., Shi, R., Zhao, G., Jiang, G.-X., Song, Y., et al. (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  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  Google Scholar 

  • Zoni, S., Albini, E., & Lucchini, R. (2007). Neuropsychological testing for the assessment of manganese neurotoxicity: A review and a proposal. American Journal of Industrial Medicine, 50(11), 812–830. https://doi.org/10.1002/ajim.20518.

    Article  PubMed  Google Scholar 

  • Zoni, S., & Lucchini, R. G. (2013). Manganese exposure: cognitive, motor and behavioral effects on children: A review of recent findings. Current Opinion in Pediatrics, 25(2), 255.

    Article  Google Scholar 

Download references

Acknowledgements

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 (UL1 TR003167) by the National Center for Advancing Translational Sciences (NCATS). Furthermore, we acknowledge that the collection and management of survey data were 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 NICHD, NIH-FIC, NIEHS, NCRR, or NCATS. Finally, we acknowledge contributions by colleagues in the Analytical Chemistry Lab at MDHHS for analyzing and storing the whole blood samples for the assessments of Mn concentrations, under a service contract.

Author information

Authors and Affiliations

Authors

Contributions

MHR is Principal Investigator (PI) of the ERAJ study from which these data originated and is responsible for designing, obtaining funding and execution of this project. MHR is also primarily responsible for analyzing the data, interpreting the findings, and revising the manuscript. MSV is co-investigator and PI of subcontract to the UWI for the ERAJ study and is responsible for designing the study and providing oversight to our study team in Jamaica. MSV also participated in revising the manuscript. SS significantly contributed to analyzing the data, interpreting the findings, drafting and revising the manuscript. ML was the statistician in the ERAJ study and participated in interpreting the findings and revising the manuscript. JB and KL are co-Investigators of the ERAJ study who contributed to study design and participated in revising the manuscript. JZ participated in analyzing the data and interpreting the findings. MH is responsible for data management of the ERAJ study 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. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Mohammad H. Rahbar.

Ethics declarations

Conflict of interest

Mohammad H. Rahbar, Maureen Samms-Vaughan, Sepideh Saroukhani, MinJae Lee, Jing Zhang, Jan Bressler, Manouchehr Hessabi, Sydonnie Shakespeare-Pellington, Megan L. Grove, Katherine A. Loveland declares that they 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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahbar, M.H., Samms-Vaughan, M., Saroukhani, S. et al. Interaction of Blood Manganese Concentrations with GSTT1 in Relation to Autism Spectrum Disorder in Jamaican Children. J Autism Dev Disord 51, 1953–1965 (2021). https://doi.org/10.1007/s10803-020-04677-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-020-04677-z

Keywords

Navigation