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Pre-conceptional and prenatal exposure to secondhand smoke and autism spectrum disorder: a national multi-center study in China

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Abstract

Background

Despite extensive research evaluating the association between prenatal exposure to secondhand smoke (SHS) and the development of autism spectrum disorders (ASD), no study has investigated the association by considering the pre-conceptional period. This study aimed to investigate the associations of pre-conceptional and prenatal SHS exposure and the development of ASD among toddlers.

Methods

In this cross-sectional study, parents of 6049 toddlers aged 16–30 months were recruited from 7 tertiary hospitals, 21 communities, and 7 kindergartens located in seven cities in six provinces from five geographical regions of China. We analyzed the associations of SHS exposure and the odds of ASD among toddlers in different exposure windows (pre-conceptional and/or prenatal periods). Data were analyzed from November 2021 to January 2022.

Results

Among the 6049 toddlers included in the analysis [22.7 (4.1) months; 44.8% girls], 71 were identified and diagnosed with ASD. Compared with the unexposed toddlers, toddlers with pre-conceptional SHS exposure had higher odds of ASD (OR 2.30, 95% CI 1.36–3.84), while we observed a non-significantly positive association regarding prenatal SHS exposure. When considering both pre-conceptional and prenatal periods, toddlers who were continuously exposed to SHS during these two periods had higher odds than those without SHS exposure (OR 2.32, 95% CI 1.24–4.14).

Conclusion

We reported positive SHS–ASD associations when exposed during the pre-conceptional period and continuously exposed during pre-conceptional and prenatal periods, emphasizing the critical window of pre-conception for targeted intervention on smoking.

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Data availability statement

Data will be made available on reasonable request from corresponding authors by email.

References

  1. Kim JY, Son MJ, Son CY, Radua J, Eisenhut M, Gressier F, et al. Environmental risk factors and biomarkers for autism spectrum disorder: an umbrella review of the evidence. Lancet Psychiatry. 2019;6:590–600.

    Article  PubMed  Google Scholar 

  2. Tang SM, Wang Y, Gong X, Wang GH. A meta-analysis of maternal smoking during pregnancy and autism spectrum disorder risk in offspring. Int J Environ Res Public Health. 2015;12:10418–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Jung Y, Lee AM, McKee SA, Picciotto MR. Maternal smoking and autism spectrum disorder: meta-analysis with population smoking metrics as moderators. Sci Rep. 2017;7:4315.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chinese Center for Disease Control and Prevention. Fact sheet of the 2018 China Adult Tobacco Survey. 2019. https://www.chinacdc.cn/jkzt/sthd_3844/slhd_12885/201908/t20190814_204616.html. Accessed 27 Feb 2022.

  5. World Health Organization. WHO report on the global tobacco epidemic, 2019: offer help to quit tobacco use. 2019. https://apps.who.int/iris/handle/10665/325968. Accessed 27 Feb 2022.

  6. Jung Y, Hsieh LS, Lee AM, Zhou Z, Coman D, Heath CJ, et al. An epigenetic mechanism mediates developmental nicotine effects on neuronal structure and behavior. Nat Neurosci. 2016;19:905–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pistillo F, Clementi F, Zoli M, Gotti C. Nicotinic, glutamatergic and dopaminergic synaptic transmission and plasticity in the mesocorticolimbic system: focus on nicotine effects. Prog Neurobiol. 2015;124:1–27.

    Article  CAS  PubMed  Google Scholar 

  8. Kim K, Lim MH, Kwon HJ, Yoo SJ, Kim EJ, Kim JWS, et al. Associations between urinary cotinine and symptoms of attention deficit/hyperactivity disorder and autism spectrum disorder. Environ Res. 2018;166:481–6.

    Article  CAS  PubMed  Google Scholar 

  9. Larsson M, Weiss B, Janson S, Sundell J, Bornehag CG. Associations between indoor environmental factors and parental-reported autistic spectrum disorders in children 6–8 years of age. Neurotoxicology. 2009;30:822–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Duan GQ, Yao ML, Ma YT, Zhang WJ. Perinatal and background risk factors for childhood autism in central China. Psychiatry Res. 2014;220:410–7.

    Article  PubMed  Google Scholar 

  11. Kaur B. The Association between autism spectrum disorders and secondhand tobacco exposure. 2014. https://corescholar.libraries.wright.edu/mph/119/. Accessed 27 Feb 2022.

  12. Khalil N, Kaur B, Lawson A, Ebert J, Nahhas R. Secondhand smoke exposure is associated with autism spectrum disorder in US males but not in females: results from the National Survey on Children’s Health. Environ Dis. 2018;3:8–17.

    Article  Google Scholar 

  13. Pham C, Symeonides C, O’Hely M, Sly PD, Knibbs LD, Thomson S, et al. Early life environmental factors associated with autism spectrum disorder symptoms in children at age 2 years: a birth cohort study. Autism. 2022;26:1864–81.

    Article  PubMed  Google Scholar 

  14. Gibson L, Porter M. Alcohol and tobacco use while breastfeeding and risk of autism spectrum disorder or attention deficit/hyperactivity disorder. J Autism Dev Disord. 2022;52:1223–34.

    Article  PubMed  Google Scholar 

  15. Bolte EE, Moorshead D, Aagaard KM. Maternal and early life exposures and their potential to influence development of the microbiome. Genome Med. 2022;14:4.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Breuss MW, Antaki D, George RD, Kleiber M, James KN, Ball LL, et al. Autism risk in offspring can be assessed through quantification of male sperm mosaicism. Nat Med. 2020;26:143–50.

    Article  CAS  PubMed  Google Scholar 

  17. Greenblatt EJ, Spradling AC. Fragile X mental retardation 1 gene enhances the translation of large autism-related proteins. Science. 2018;361:709–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Zhang X, Lv CC, Tian J, Miao RJ, Xi W, Hertz-Picciotto I, et al. Prenatal and perinatal risk factors for autism in China. J Autism Dev Disord. 2010;40:1311–21.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Mrozek-Budzyn D, Majewska R, Kieltyka A. Prenatal, perinatal and neonatal risk factors for autism—study in Poland. Cent Eur J Med. 2013;8:424–30.

    Google Scholar 

  20. Nani D, Herini ES, Sadewa AH, Hartini S, Putri DA, Kusumawardani LH. Prenatal and neonatal factors related with autism spectrum disorder: a case-control study in Banyumas, Central Java, Indonesia. Ann Trop Med Public Health. 2019;22:11.

    Article  Google Scholar 

  21. Cheslack-Postava K, Sourander A, Hinkka-Yli-Salomaki S, McKeague IW, Surcel HM, Brown AS. A biomarker-based study of prenatal smoking exposure and autism in a Finnish national birth cohort. Autism Res. 2021;14:2444–53.

    Article  PubMed  Google Scholar 

  22. Berger K, Pearl M, Kharrazi M, Li Y, DeGuzman J, She J, et al. The association of in utero tobacco smoke exposure, quantified by serum cotinine, and Autism Spectrum Disorder. Autism Res. 2021;14:2017–26.

    Article  PubMed  Google Scholar 

  23. Jo H, Eckel SP, Wang X, Chen JC, Cockburn M, Martinez MP, et al. Sex-specific associations of autism spectrum disorder with residential air pollution exposure in a large Southern California pregnancy cohort. Environ Pollut. 2019;254:113010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Pagalan L, Bickford C, Weikum W, Lanphear B, Brauer M, Lanphear N, et al. Association of prenatal exposure to air pollution with autism spectrum disorder. JAMA Pediatr. 2019;173:86–92.

    Article  PubMed  Google Scholar 

  25. Guo CH, Luo MF, Wang XX, Huang SJ, Meng ZX, Shao J, et al. Reliability and validity of the chinese version of modified checklist for autism in toddlers, revised, with follow-up (M-CHAT-R/F). J Autism Dev Disord. 2019;49:185–96.

    Article  PubMed  Google Scholar 

  26. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche ZC, Vandenbroucke JP. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ. 2007;335:806–8.

    Article  Google Scholar 

  27. Pierce K, Gazestani VH, Bacon E, Barnes CC, Cha D, Nalabolu S, et al. Evaluation of the diagnostic stability of the early autism spectrum disorder phenotype in the general population starting at 12 months. JAMA Pediatr. 2019;173:578–87.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lu JT, Yang ZW, Shu MY, Su LY. Reliability, validity analysis of the childhood autism rating scale. Journal. 2004;14:119–21, 123.

    Google Scholar 

  29. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. 2013. https://www.psychiatry.org/psychiatrists/practice/dsm/updates-to-dsm-5//updates-to-dsm-5-criteria-text. Accessed 27 Feb 2022.

  30. National Health Commission of the People's Republic of China. Criteria of weight for adults, people's health industry standards of People's Republic of China. 2013. http://www.nhc.gov.cn/wjw/yingyang/201308/a233d450fdbc47c5ad4f08b7e394d1e8.shtml. Accessed 27 Feb 2022.

  31. Puhr R, Heinze G, Nold M, Lusa L, Geroldinger A. Firth’s logistic regression with rare events: accurate effect estimates and predictions? Stat Med. 2017;36:2302–17.

    PubMed  Google Scholar 

  32. Johani FH, Mohamed NE, Abd Majid MS, Ibrahim SD, Isa ZM. Secondhand smoke exposure and autism spectrum disorder: a meta-analysis. Sains Malays. 2020;49:1615–25.

    Article  CAS  Google Scholar 

  33. Banderali G, Martelli A, Landi M, Moretti F, Betti F, Radaelli G, et al. Short and long term health effects of parental tobacco smoking during pregnancy and lactation: a descriptive review. J Transl Med. 2015;13:327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chang RC, Ho YS, Wong S, Gentleman SM, Ng HK. Neuropathology of cigarette smoking. Acta Neuropathol. 2014;127:53–69.

    Article  CAS  PubMed  Google Scholar 

  35. Colombo G, Clerici M, Giustarini D, Portinaro NM, Aldini G, Rossi R, et al. Pathophysiology of tobacco smoke exposure: recent insights from comparative and redox proteomics. Mass spectrom Rev. 2014;33:183–218.

    Article  CAS  PubMed  Google Scholar 

  36. Torabi R, Jenkins S, Harker A, Whishaw IQ, Gibb R, Luczak A. A neural network reveals motoric effects of maternal preconception exposure to nicotine on rat pup behavior: a new approach for movement disorders diagnosis. Front Neurosci. 2021;15:686767.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Zenzes MT. Smoking and reproduction: gene damage to human gametes and embryos. Hum Reprod Update. 2000;6:122–31.

    Article  CAS  PubMed  Google Scholar 

  38. Sharma R, Harlev A, Agarwal A, Esteves SC. Cigarette smoking and semen quality: a new meta-analysis examining the effect of the 2010 World Health Organization laboratory methods for the examination of human semen. Eur Urol. 2016;70:635–45.

    Article  PubMed  Google Scholar 

  39. Ma C, Heiland EG, Li Z, Zhao M, Liang Y, Xi B. Global trends in the prevalence of secondhand smoke exposure among adolescents aged 12–16 years from 1999 to 2018: an analysis of repeated cross-sectional surveys. Lancet Glob Health. 2021;9:e1667–78.

    Article  CAS  PubMed  Google Scholar 

  40. Yang L, Wu H, Zhao M, Magnussen CG, Xi B. Prevalence and trends in tobacco use, secondhand smoke exposure at home and household solid fuel use among women in 57 low- and middle-income countries, 2000–2018. Environ Int. 2022;161:107142.

    Article  PubMed  Google Scholar 

  41. Mao A, Bottorff JL, Oliffe JL, Sarbit G, Kelly MT. A qualitative study of Chinese Canadian fathers’ smoking behaviors: intersecting cultures and masculinities. BMC Public Health. 2015;15:286.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Flemming K, Graham H, McCaughan D, Angus K, Bauld L. The barriers and facilitators to smoking cessation experienced by women’s partners during pregnancy and the post-partum period: a systematic review of qualitative research. BMC Public Health. 2015;15:849.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Avila-Tang E, Elf JL, Cummings KM, Fong GT, Hovell MF, Klein JD, et al. Assessing secondhand smoke exposure with reported measures. Tob Control. 2013;22:156–63.

    Article  PubMed  Google Scholar 

  44. Zhou H, Xu X, Yan W, Zou X, Wu L, Luo X, et al. Prevalence of autism spectrum disorder in China: a nationwide multi-center population-based study among children aged 6 to 12 years. Neurosci Bull. 2020;36:961–71.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Dai Q, Xu HQ, Wang H, Zhao ZW, Zhang X, Zhou AQ. Prevalence of autism spectrum disorder in Chinese children from 2000 to 2016: a meta-analysis. Chin J Child Health Care. 2017;25:1243–6.

    Google Scholar 

  46. Halladay AK, Bishop S, Constantino JN, Daniels AM, Koenig K, Palmer K, et al. Sex and gender differences in autism spectrum disorder: summarizing evidence gaps and identifying emerging areas of priority. Mol Autism. 2015;6:36.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

None.

Funding

This work was supported by the Key-Area Research and Development Program of Guangdong Province, China (2019B030335001), the National Natural Science Foundation of China, China (82103794), and the National Social Science Foundation of China (20&ZD296).

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Authors and Affiliations

Authors

Contributions

LLZ: conceptualization, supervision, project administration, funding acquisition, methodology, formal analysis, software, validation, resources, investigation, data curation, writing–original draft, writing–review and editing. OXX: methodology, formal analysis, software, validation, resources, investigation, data curation, writing—original draft, writing—review and editing. ZXL: investigation, writing–review and editing. WX: software, validation, resources, investigation, writing–review and editing. CL, LXH: writing–review and editing. DGH, JJ: conceptualization, supervision, project administration, funding acquisition, writing–review and editing. LLZ and OXX contributed equally to this work and should be listed as the first author.

Corresponding authors

Correspondence to Jin Jing or Guang-Hui Dong.

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Conflict of interest

No financial or non-financial benefits have been received or will be received from any party related directly or indirectly to the subject of this article. None of any authors serves as a current Editorial Team member (such as Chief Editors, Deputy Chief Editors, Associate Editors, Editorial Board Member) for this journal.

Ethical approval

This study was approved by the Ethical Review Committee for Biomedical Research, Sun Yat-sen University. Informed consent to participate in the study has been obtained from participants (or their parent or legal guardian in the case of children under 16).

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Lin, LZ., Ou, XX., Zhan, XL. et al. Pre-conceptional and prenatal exposure to secondhand smoke and autism spectrum disorder: a national multi-center study in China. World J Pediatr 19, 761–769 (2023). https://doi.org/10.1007/s12519-022-00644-z

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