Association of physical activity and sleep habits during pregnancy with autistic spectrum disorder in 3-year-old infants

1.

Ministry of Education, Culture, Sports, Science and Technology of Japan.

Number of students taking special classes in 2014. page 1, Figure. Changes in the

number of students taking special class from 1993 to 2014 (in Japanese). https://

www.mext.go.jp/a_menu/shotou/tokubetu/material/__icsFiles/afieldfile/2015/

03/27/1356210.pdf. (2014).

2. Schendel, D. E. & Thorsteinsson, E. Cumulative incidence of autism into

adulthood for birth cohorts in Denmark, 1980-2012. JAMA 320, 1811–1813

(2018).

3. Zablotsky, B. et al. Prevalence and trends of developmental disabilities among

children in the United States: 2009–2017. Pediatrics 144, 2009–2017 (2019).

4. Chaste, P. & Leboyer, M. Autism risk factors: genes, environment, and geneenvironment interactions. Dialogues Clin. Neurosci. 14, 281–292 (2012).

5. Gardener, H., Spiegelman, D. & Buka, S. L. Perinatal and neonatal risk factors

for autism: a comprehensive meta-analysis. Pediatrics 128, 344–355 (2011).

6. van Hoorn, J. F. et al. Risk factors in early life for developmental coordination

disorder: a scoping review. Dev. Med. Child Neurol. 63, 511–519 (2021).

7. Álvarez-Bueno, C. et al. Pregnancy leisure physical activity and children’s

neurodevelopment: a narrative review. BJOG Int. J. Obstet. Gynaecol. 125,

1235–1242 (2018).

8. Niño Cruz, G. I., Ramirez Varela, A., da Silva, I. C. M., Hallal, P. C. & Santos,

I. S. Physical activity during pregnancy and offspring neurodevelopment: a

systematic review. Paediatr. Perinat. Epidemiol. 32, 369–379 (2018).

9. Facco, F. L. et al. Association of adverse pregnancy outcomes with selfreported measures of sleep duration and timing in women who are

nulliparous. J. Clin. Sleep Med. 14, 2047–2056 (2018).

10. Pauley, A. M. et al. Short nighttime sleep duration and high number of

nighttime awakenings explain increases in gestational weight gain and

decreases in physical activity but not energy intake among pregnant women

with overweight/obesity. Clocks Sleep 2, 487–501 (2020).

11. Wang, C., Geng, H., Liu, W. & Zhang, G. Prenatal, perinatal, and postnatal

factors associated with autism: a meta-analysis. Medicine (United States) 96,

1–7 (2017).

12. Acosta-Manzano et al. Influence of a concurrent exercise training intervention

during pregnancy on maternal and arterial and venous cord serum cytokines:

The GESTAFIT Project. J. Clin. Med. 8, 1862 (2019).

13. Gleeson, M. et al. The anti-inflammatory effects of exercise: mechanisms and

implications for the prevention and treatment of disease. Nat. Rev. Immunol.

11, 607–610 (2011).

14. Irwin, M. R., Olmstead, R. & Carroll, J. E. Sleep disturbance, sleep duration,

and inflammation: a systematic review and meta-analysis of cohort studies

and experimental sleep deprivation. Biol. Psychiatry 80, 40–52 (2016).

15. Tobaldini, E. et al. Short sleep duration and cardiometabolic risk: from

pathophysiology to clinical evidence. Nat. Rev. Cardiol. 16, 213–224 (2019).

16. Estes, M. L. & McAllister, A. K. Maternal immune activation: Implications for

neuropsychiatric disorders. Science 353, 772–777 (2016).

17. Schobel, S. A. et al. Maternal immune activation and abnormal brain

development across CNS disorders. Nat. Rev. Neurol. 10, 643–660 (2014).

18. Myers, J., Kokkinos, P. & Nyelin, E. Physical activity, cardiorespiratory fitness,

and the metabolic syndrome. Nutrients 11, 1–18 (2019).

19. Xu, Y. H. et al. Association between sleep duration during pregnancy and

gestational diabetes mellitus: a meta-analysis. Sleep Med. 52, 67–74 (2018).

20. Williams, M. A. et al. Associations of early pregnancy sleep duration with

trimester-specific blood pressures and hypertensive disorders in pregnancy.

Sleep 33, 1363–1371 (2010).

21. Palagini, L. et al. Chronic sleep loss during pregnancy as a determinant of

stress: impact on pregnancy outcome. Sleep Med. 15, 853–859 (2014).

22. Russo, L. M., Nobles, C., Ertel, K. A., Chasan-Taber, L. & Whitcomb, B. W.

Physical activity interventions in pregnancy and risk of gestational diabetes

mellitus a systematic review and meta-analysis. Obstet. Gynecol. 125, 576–582

(2015).

23. Di Mascio, D., Magro-Malosso, E. R., Saccone, G., Marhefka, G. D. &

Berghella, V. Exercise during pregnancy in normal-weight women and risk of

preterm birth: a systematic review and meta-analysis of randomized

controlled trials. Am. J. Obstet. Gynecol. 215, 561–571 (2016).

24. Nakahara, K. et al. Influence of physical activity before and during pregnancy

on infant’s sleep and neurodevelopment at 1-year-old. Sci. Rep. 11, 1–11

(2021).

25. Nakahara, K. et al. Association of maternal sleep before and during pregnancy

with sleep and developmental problems in 1 ‑ year ‑ old infants. Sci. Rep. 11,

1–16 (2021).

26. Zwaigenbaum, L. et al. Clinical assessment and management of toddlers with

suspected autism spectrum disorder: Insights from studies of high-risk infants.

Pediatrics 123, 1383–1391 (2009).

27. Francesco, P., Maria, R. & L., P. Sleep habits in children affected by autism

spectrum disorders: a preliminary case-control study. Acta Medica Mediterr

33, 405–409 (2017).

28. Richdale, A. L. & Prior, M. R. The sleep/wake rhythm in children with autism.

Eur. Child Adolesc. Psychiatry 4, 175–186 (1995).

29. Kawamoto, T. et al. Rationale and study design of the Japan environment and

children’s study (JECS). BMC Public Health 14, 25 (2014).

30. Michikawa, T. et al. Baseline profile of participants in the Japan Environment

and Children’s Study (JECS). J. Epidemiol. 28, 99–104 (2018).

31. Craig, C. L. et al. International physical activity questionnaire: 12-Country

reliability and validity. Med. Sci. Sports Exerc. 35, 1381–1395 (2003).

32. Murase, N. et al. Validity and reliability of Japanese version of international

physical activity questionnaire. J Health Welfare Stat. 49, 1–9 (2002).

33. Kurita, H., Koyama, T. & Osada, H. Autism-Spectrum Quotient-Japanese

version and its short forms for screening normally intelligent persons with

pervasive developmental disorders. Psychiatry Clin. Neurosci. 59, 490–496

(2005).

34. Daniels, J. L. et al. Parental psychiatric disorders associated with autism

spectrum disorders in the offspring. Pediatrics 121, 1357–1362 (2008).

35. Wiggins, L. D. et al. A phenotype of childhood autism is associated with

preexisting maternal anxiety and depression. J Abnorm. Child Psychol. 47,

731–740 (2019).

36. Bassan, H. et al. The effect of maternal sleep-disordered breathing on the

infant’s neurodevelopment. Am. J. Obstet. Gynecol. 212, 656.e1–656.e7 (2015).

37. Sun, Y., Hons, B., Cistulli, P. A. & Hons, M. Childhood health and educational

outcomes associated with maternal sleep apnea: a population record-linkage

study. Sleep 40, zsx158 (2014).

38. Grieger, J. A. et al. Metabolic syndrome in pregnancy and risk for adverse

pregnancy outcomes: A prospective cohort of nulliparous women. PLoS Med.

15, 1–16 (2018).

39. Contu, L. & Hawkes, C. A. A review of the impact of maternal obesity on the

cognitive function and mental health of the offspring. Int. J. Mol. Sci. 18, 1093

(2017).

40. Edlow, A. G. Maternal obesity and neurodevelopmental and psychiatric

disorders in offspring. Prenat. Diagn. 37, 95–110 (2017).

41. Saito, M. et al. Prevalence and cumulative incidence of autism spectrum

disorders and the patterns of co-occurring neurodevelopmental disorders in a

total population sample of 5-year-old children. Mol. Autism. 11, 1–9 (2020).

COMMUNICATIONS MEDICINE | (2022)2:35 | https://doi.org/10.1038/s43856-022-00101-y | www.nature.com/commsmed

COMMUNICATIONS MEDICINE | https://doi.org/10.1038/s43856-022-00101-y

42. Honda, H., Shimizu, Y., Imai, M. & Nitto, Y. Cumulative incidence of

childhood autism: a total population study of better accuracy and precision.

Dev. Med. Child Neurol. 47, 10–18 (2005).

43. Kamio, Y. et al. Effectiveness of using the modified checklist for autism in

toddlers in two-stage screening of autism spectrum disorder at the 18-month

health check-up in Japan. J. Autism Dev. Disord. 44, 194–203 (2014).

Acknowledgements

We would like to express our gratitude to all the participants of this study and all

individuals involved in data collection. The Japan Environment and Children’s Study was

funded by the Ministry of Environment, Japan. The findings and conclusions of this

article are solely the responsibility of the authors and do not represent the official views

of the above government. This work was inspired by other works supported by the

RIKEN Healthcare and Medical Data Platform Project and JSPS KAKENHI (grant

numbers: JP16H01880, JP16K13072, JP18H00994, and JP18H03388).

Author contributions

Study conception and design: S.M. Statistical analyses: T.M. Drafting of the manuscript

and approval of final content: K.N., S.M., and T.M. Critical revision of the manuscript for

important intellectual content and manuscript review: K.N., T.M., S.M., N.H., M.O., K.K.

(Kiyoko Kato), M.S. (Masafumi Sanefuji), E.S., M.T., M.S. (Masayuki Shimono), T.K.,

S.O., K.K. (Koichi Kusuhara), and JECS group members.

ARTICLE

Additional information

Supplementary information The online version contains supplementary material

available at https://doi.org/10.1038/s43856-022-00101-y.

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Peer review information Communications Medicine thanks Pedro Hallal and the other,

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Competing interests

The authors declare no competing interests.

© The Author(s) 2022

the Japan Environment and Children’s Study Group

Michihiro Kamijima10, Shin Yamazaki11, Yukihiro Ohya12, Reiko Kishi13, Nobuo Yaegashi14, Koichi Hashimoto15,

Chisato Mori16, Shuichi Ito17, Zentaro Yamagata18, Hidekuni Inadera19, Takeo Nakayama20, Hiroyasu Iso21,

Masayuki Shima22, Youichi Kurozawa23, Narufumi Suganuma24 & Takahiko Katoh25

10

Nagoya City University, Nagoya, Japan. 11National Institute for Environmental Studies, Tsukuba, Japan. 12National Center for Child Health and

Development, Tokyo, Japan. 13Hokkaido University, Sapporo, Japan. 14Tohoku University, Sendai, Japan. 15Fukushima Medical University,

Fukushima, Japan. 16Chiba University, Chiba, Japan. 17Yokohama City University, Yokohama, Japan. 18University of Yamanashi, Chuo, Japan.

19

University of Toyama, Toyama, Japan. 20Kyoto University, Kyoto, Japan. 21Osaka University, Suita, Japan. 22Hyogo College of Medicine,

Nishinomiya, Japan. 23Tottori University, Yonago, Japan. 24Kochi University, Nankoku, Japan. 25Kumamoto University, Kumamoto, Japan.

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