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. 2021 Apr 14;11:8099. doi: 10.1038/s41598-021-87612-1

Influence of physical activity before and during pregnancy on infant’s sleep and neurodevelopment at 1-year-old

Kazushige Nakahara 1,#, Takehiro Michikawa 2,#, Seiichi Morokuma 3,4,✉, Masanobu Ogawa 4, Kiyoko Kato 1,4, Masafumi Sanefuji 4,5, Eiji Shibata 6,7, Mayumi Tsuji 6,8, Masayuki Shimono 6,9, Toshihiro Kawamoto 6, Shouichi Ohga 5, Koichi Kusuhara 6,9; the Japan Environment and Children’s Study Group
PMCID: PMC8046980  PMID: 33854123

Abstract

The aim of this study was to investigate the association between maternal physical activity (PA) before and during pregnancy and sleep and developmental problems in 1-year-old infants. We used data from a nationwide cohort study in Japan that registered 103,062 pregnancies between 2011 and 2014. Participants were asked about their PA before and during pregnancy, and the sleep and development of their children at the age of 1 year. Maternal PA was estimated using the International Physical Activity Questionnaire and was expressed in METs per week. We defined scores below the cut-off points of the Ages and Stages Questionnaire (ASQ) as abnormal for infant development. Based on the levels of PA before or during pregnancy, the participants were divided into five groups. In mothers with higher PA levels, the risk ratio for bedtime after 22:00 or abnormal ASQ scores in their 1-years-old infants were lower. These associations were observed for PA before and during pregnancy. Higher levels of maternal PA, both before and during pregnancy, may reduce sleep and developmental problems in infants.

Subject terms: Health care, Medical research, Risk factors

Introduction

Many previous studies have reported that maternal physical activity (PA) and exercise during pregnancy are associated with decreases in various perinatal outcomes, such as gestational diabetes mellitus (GDM)1, hypertensive disorders of pregnancy (HDP)2, and risk for cesarean section3,4. In recent years, a positive association between PA during pregnancy and infant development has been reported. Two review articles in 2018 concluded that PA during pregnancy was associated with improved language development5 and total neurodevelopment6. To our knowledge, no published studies have reported the association between maternal PA or exercise before pregnancy and infant neurodevelopment.

Recently, the importance of preconception care has become more recognized7–9. For example, moderate exercise prior to conception is recommended by the American College of Obstetricians and Gynecologists8. However, the publication focused on the benefits of exercising for improving obesity and reducing perinatal complications, and the statement did not mention infant development. It has also been reported that exercise before pregnancy reduces GDM10 . GDM increases the risk of developmental disorders11; therefore, the level of PA or exercise during preconception may affect infant development. Children with developmental disorders, such as autism, tend to have sleeping problems, including frequent awakening, crying during the night, and short sleep time due to late bedtime12,13. These children also tend to experience developmental delays during early infancy14. To our knowledge, no published studies have reported the effects of maternal PA before or during pregnancy on infant sleep. We hypothesize that higher maternal PA before and during pregnancy may improve sleep and neurodevelopment in infants.

This study aimed to investigate the association between maternal PA before and during pregnancy, and infant sleep and developmental problems at 1-year-old using large-scale data.

Results

The baseline characteristics of the participants, along with the available data on maternal PA before pregnancy, are shown in Table 1. The characteristics of the participants with available data during pregnancy are shown in Table S1. The median (interquartile range) levels of PA before and during pregnancy were 854 (196–2975) METs-min/week and 497 (63–1386) METs-min/week, respectively.

Table 1.

Baseline characteristics of the study population categorized by physical activity before pregnancy.

Physical activity before pregnancy
PA = 0 Quartile 1 Quartile 2 Quartile 3 Quartile 4
n* % n* % n* % n* % n* %
Physical activity, median (IQR), METs・min/week 0 245 (168–385) 791 (602–987) 2163 (1617–2968) 8078 (5789–12,313)
Maternal characteristics
 Age at delivery (years)
   < 25 1054 8.1 984 6.5 1039 6.5 1318 8.5 2206 14.5
  25–29 3407 26.2 3860 25.3 4133 25.8 4339 28.0 4959 32.6
  30–34 4654 35.8 5722 37.5 6013 37.5 5643 36.4 4983 32.8
   ≥ 35 3869 29.8 4689 30.7 4846 30.2 4184 27.0 3069 20.2
Smoking habits
Never smoked 7661 59.1 9633 63.2 10196 63.7 9198 59.5 8006 52.7
Ex-smokers who quit before pregnancy 2908 22.4 3555 23.3 3781 23.6 3825 24.7 3546 23.3
Smokers during early pregnancy 2392 18.5 2051 13.5 2043 12.8 2443 15.8 3645 24.0
Alcohol consumption
Never drank 5002 38.5 5349 35.1 5329 33.3 5111 33.0 5027 33.1
Ex-drinkers who quit before pregnancy 2134 16.4 2845 18.7 3004 18.7 2923 18.9 2766 18.2
Drinkers during early pregnancy 5846 45.0 7059 46.3 7694 48.0 7446 48.1 7418 48.8
Pre-pregnancy body mass index (kg/m2)
 < 18.5 2191 16.9 2575 16.9 2469 15.4 2405 15.5 2400 15.8
18.5–24.9 9541 73.5 11209 73.5 12037 75.1 11534 74.5 11154 73.3
 ≥ 25.0 1252 9.6 1464 9.6 1513 9.5 1539 9.9 1660 10.9
Parity
0 6065 46.8 6530 43.0 6900 43.2 6227 40.4 7548 49.8
 ≥ 1 6885 53.2 8673 57.1 9,077 56.8 9,197 59.6 7,625 50.3
Infertility treatment
No 12,098 93.2 14,059 92.2 14,771 92.2 14,475 93.5 14,468 95.1
Ovulation stimulation/artificial insemination using husband’s sperms 471 3.6 635 4.2 648 4.0 574 3.7 467 3.1
Assisted reproductive technology 415 3.2 556 3.7 605 3.8 429 2.8 277 1.8
Current history
Hypertensive disorders during pregnancy 421 3.2 362 2.4 415 2.6 379 2.5 501 3.3
Diabetes or gestational diabetes 379 2.9 451 3.0 499 3.1 477 3.1 447 2.9
Type of delivery
Vaginal 10,623 81.9 12,602 82.8 13,285 83.1 12,765 82.6 12,648 83.3
Caesarean 2,345 18.1 2,617 17.2 2,710 16.9 2,685 17.4 2,536 16.7
Gestational age (weeks)
Early term (37–38) 4,249 32.7 4,967 32.6 5,231 32.6 5,218 33.7 4,820 31.7
Full term (39–41) 8,735 67.3 10,288 67.4 10,800 67.4 10,266 66.3 10,397 68.3
K6 Scale at 1 year after delivery
0–4 10,228 78.9 12,022 78.9 12,597 78.7 11,973 77.4 11,579 76.2
 ≥ 5 (psychological distress) 2728 21.1 3212 21.1 3413 21.3 3491 22.6 3612 23.8
Educational background (years)
 < 10 464 3.6 455 3.0 540 3.4 635 4.1 917 6.1
10–12 4500 34.9 4271 28.2 4210 26.5 4445 28.9 5213 34.6
13–16 7,801 60.5 10,148 67.0 10,784 67.9 9,985 65.0 8,825 58.5
 ≥ 17 125 1.0 271 1.8 355 2.2 292 1.9 123 0.8
Household income (million Japanese yen/year)
 < 2 645 5.4 595 4.2 597 4.0 680 4.7 1,086 7.8
2 to < 4 3995 33.4 4591 32.0 4687 31.2 4932 34.1 5508 39.4
4 to < 6 4005 33.5 5003 34.9 5210 34.7 4910 34.0 4245 30.3
6 to < 8 2040 17.0 2409 16.8 2650 17.7 2352 16.3 1895 13.5
8 to < 10 827 6.9 1038 7.2 1105 7.4 945 6.5 819 5.9
 ≥ 10 457 3.8 710 5.0 761 5.1 645 4.5 440 3.1
Infant characteristics
 Birth weight
  Mean (SD) (g) 3054 (362) 3065 (360) 3065 (368) 3066 (364) 3056 (368)
  Small for gestational age 949 7.3 1,015 6.7 1,198 7.5 1,063 6.9 1,196 7.9
 Infant sex
  Male 6,582 50.7 7,723 50.6 8,226 51.3 7,888 50.9 7,773 51.1
  Female 6,402 49.3 7,532 49.4 7,805 48.7 7,596 49.1 7,444 48.9
Doctor diagnosis at 1-year-old
Asthma 305 2.4 325 2.1 351 2.2 360 2.3 481 3.2
Atopic dermatitis 516 4.0 654 4.3 744 4.6 649 4.2 723 4.8
Feeding status
Formula feeding 378 2.9 296 1.9 299 1.9 273 1.8 381 2.5
Partial breastfeeding 8639 66.5 9740 63.9 10,046 62.7 9635 62.2 10,050 66.0
Exclusive breastfeeding 3967 30.6 5219 34.2 5686 35.5 5576 36.0 4786 31.5
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*Numbers in subgroups do not equal overall number because of missing data.

PA physical activity, MET metabolic equivalent of a task, IQR interquartile range, K6 scale the Kessler six-item psychological distress scale, SD standard deviation.

Association of maternal PA before and during pregnancy with sleep problems in 1-year-old infants

Low levels of maternal PA before and during pregnancy were associated with an increased risk ratio for bedtime after 22:00 but were not associated with other sleep outcomes (Tables 2 and 3). The risk ratio of bedtime after 22:00 in the group with the highest levels of PA (Quartile 4) both before and during pregnancy was lower than the reference group (PA before pregnancy, RR = 0.91, 95% CI = 0.87–0.95; PA during pregnancy, RR = 0.88, 95% CI = 0.84–0.92).

Table 2.

Association between physical activity before pregnancy and infant sleep and development, Japan Environment and Children’s Study (2011–2014).

No. of participants No. of outcome Maternal age adjusted model Multivariable modela
% RR 95% CI RR 95% CI
Sleeping problems
 3 or more awakening times in a night
  PA = 0 12,895 280 2.2 0.95 0.81 1.11 0.98 0.84 1.15
  Quartile 1 15,158 350 2.3 Ref Ref
  Quartile 2 15,923 426 2.7 1.16 1.01 1.33 1.14 0.99 1.31
  Quartile 3 15,388 391 2.5 1.12 0.97 1.29 1.10 0.95 1.27
  Quartile 4 15,128 357 2.4 1.08 0.93 1.24 1.11 0.95 1.28
1 or more awakening times and staying awake for more than 1 h
PA = 0 12,895 736 5.7 1.08 0.98 1.19 1.05 0.95 1.16
Quartile 1 15,158 801 5.3 Ref Ref
Quartile 2 15,923 931 5.9 1.11 1.01 1.21 1.11 1.01 1.21
Quartile 3 15,388 880 5.7 1.08 0.99 1.19 1.07 0.98 1.18
Quartile 4 15,128 901 6.0 1.12 1.02 1.23 1.07 0.98 1.18
Sleep for less than 8 h during the night (20:00 to 07:59)
PA = 0 12,895 712 5.5 1.12 1.01 1.24 1.10 1.00 1.22
Quartile 1 15,158 747 4.9 Ref Ref
Quartile 2 15,923 850 5.3 1.08 0.99 1.19 1.08 0.98 1.19
Quartile 3 15,388 799 5.2 1.06 0.96 1.16 1.06 0.96 1.17
Quartile 4 15,128 782 5.2 1.05 0.95 1.16 1.01 0.92 1.12
Sleep at 22:00 or later
PA = 0 12,895 2723 21.1 1.01 0.97 1.06 0.99 0.94 1.03
Quartile 1 15,158 3140 20.7 Ref Ref
Quartile 2 15,923 3159 19.8 0.96 0.92 1.00 0.97 0.93 1.01
Quartile 3 15,388 2958 19.2 0.92 0.88 0.97 0.93 0.89 0.97
Quartile 4 15,128 2993 19.8 0.93 0.89 0.97 0.91 0.87 0.95
Crying at night for 5 or more days in a week
PA = 0 12,975 904 7.0 0.96 0.88 1.04 0.99 0.91 1.07
Quartile 1 15,250 1111 7.3 Ref Ref
Quartile 2 16,031 1227 7.7 1.05 0.97 1.14 1.05 0.97 1.13
Quartile 3 15,474 1189 7.7 1.06 0.98 1.14 1.05 0.97 1.14
Quartile 4 15,211 1093 7.2 1.00 0.92 1.08 1.02 0.94 1.10
The ages and stages questionnaire (ASQ)
 Communication
  PA = 0 11,804 12 0.1 1.11 0.51 2.44 1.13 0.51 2.47
  Quartile 1 13,953 13 0.1 Ref Ref
  Quartile 2 14,687 17 0.1 1.24 0.60 2.56 1.24 0.60 2.56
  Quartile 3 14,118 17 0.1 1.33 0.65 2.74 1.37 0.67 2.82
  Quartile 4 13,916 8 0.1 0.69 0.28 1.66 0.69 0.29 1.68
Gross motor skills
PA = 0 11,805 654 5.5 0.95 0.86 1.05 0.95 0.86 1.05
Quartile 1 13,953 820 5.9 Ref Ref
Quartile 2 14,685 825 5.6 0.96 0.87 1.05 0.97 0.88 1.06
Quartile 3 14,117 758 5.4 0.94 0.85 1.03 0.96 0.87 1.05
Quartile 4 13,920 682 4.9 0.90 0.82 1.00 0.93 0.84 1.02
Fine motor skills
PA = 0 11,800 799 6.8 1.17 1.07 1.29 1.15 1.05 1.26
Quartile 1 13,949 814 5.8 Ref Ref
Quartile 2 14,679 830 5.7 0.97 0.88 1.07 0.97 0.88 1.07
Quartile 3 14,110 755 5.4 0.94 0.85 1.03 0.93 0.85 1.03
Quartile 4 13,913 620 4.5 0.82 0.74 0.91 0.81 0.73 0.90
Problem-solving skills
PA = 0 11,784 760 6.5 1.23 1.12 1.36 1.20 1.09 1.33
Quartile 1 13,932 736 5.3 Ref Ref
Quartile 2 14,662 768 5.2 0.99 0.90 1.10 1.00 0.90 1.10
Quartile 3 14,102 629 4.5 0.86 0.78 0.96 0.87 0.79 0.97
Quartile 4 13,907 596 4.3 0.87 0.78 0.97 0.86 0.78 0.96
Personal–social characteristics
PA = 0 11,771 171 1.5 1.27 1.02 1.57 1.29 1.04 1.60
Quartile 1 13,910 161 1.2 Ref Ref
Quartile 2 14,654 167 1.1 0.99 0.80 1.22 0.99 0.80 1.23
Quartile 3 14,084 163 1.2 1.03 0.83 1.27 1.04 0.84 1.30
Quartile 4 13,887 121 0.9 0.81 0.64 1.02 0.83 0.65 1.05
Total (abnormal score for any 1 of the 5 domain)
PA = 0 11,810 1805 15.3 1.06 1.00 1.12 1.05 0.99 1.11
Quartile 1 13,958 2030 14.5 Ref Ref
Quartile 2 14,692 2013 13.7 0.94 0.89 1.00 0.95 0.89 1.00
Quartile 3 14,121 1817 12.9 0.90 0.85 0.96 0.91 0.86 0.97
Quartile 4 13,924 1582 11.4 0.84 0.79 0.89 0.84 0.79 0.90
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PA physical activity, CI confidence interval, RR risk ratio, Ref reference.

aAdjusted for maternal age at delivery, smoking habits, alcohol consumption, pre-pregnancy body mass index, gestational age at birth, parity, infertility treatment, infant sex, type of delivery, psychological distress at 1 year after delivery, diagnosis of asthma and atopic dermatitis at 1-year-old, and feeding status.

Table 3.

Association between physical activity during pregnancy and infant sleep and development, Japan Environment and Children’s Study (2011–2014).

No. of participants No. of outcome Maternal age adjusted model Multivariable modela
% RR 95% CI RR 95% CI
Sleeping problems
 3 or more awakening times in a night
  PA = 0 16,611 365 2.2 0.93 0.80 1.08 0.95 0.82 1.10
  Quartile 1 13,885 327 2.4 Ref Ref
  Quartile 2 13,107 305 2.3 0.99 0.85 1.16 0.97 0.83 1.13
  Quartile 3 14,653 403 2.8 1.18 1.02 1.36 1.16 1.00 1.34
  Quartile 4 13,991 345 2.5 1.07 0.93 1.25 1.09 0.94 1.26
1 or more awakening times and stayed awake for more than 1 h
PA = 0 16,611 958 5.8 0.99 0.90 1.08 1.00 0.91 1.09
Quartile 1 13,885 811 5.8 Ref Ref
Quartile 2 13,107 725 5.5 0.95 0.86 1.04 0.95 0.86 1.04
Quartile 3 14,653 823 5.6 0.96 0.88 1.06 0.96 0.88 1.06
Quartile 4 13,991 824 5.9 1.01 0.92 1.11 1.01 0.92 1.11
Sleep for less than 8 h during the night (20:00 to 7:59)
PA = 0 16,611 860 5.2 0.98 0.89 1.08 0.99 0.90 1.09
Quartile 1 13,885 732 5.3 Ref Ref
Quartile 2 13,107 693 5.3 1.01 0.91 1.11 1.00 0.90 1.10
Quartile 3 14,653 770 5.3 1.00 0.91 1.11 1.00 0.91 1.10
Quartile 4 13,991 731 5.2 1.00 0.91 1.11 1.01 0.91 1.11
Sleep at 22:00 or later
PA = 0 16,611 3367 20.3 0.96 0.92 1.00 0.95 0.91 0.99
Quartile 1 13,885 2945 21.2 Ref Ref
Quartile 2 13,107 2667 20.4 0.96 0.92 1.01 0.96 0.91 1.00
Quartile 3 14,653 2976 20.3 0.96 0.91 1.00 0.96 0.91 1.00
Quartile 4 13,991 2626 18.8 0.88 0.84 0.92 0.88 0.84 0.92
Crying at night for 5 or more days in a week
PA = 0 16,721 1197 7.2 0.96 0.88 1.03 0.98 0.90 1.06
Quartile 1 13,967 1046 7.5 Ref Ref
Quartile 2 13,192 1008 7.6 1.02 0.94 1.11 1.01 0.93 1.10
Quartile 3 14,731 1096 7.4 0.99 0.92 1.08 0.99 0.91 1.07
Quartile 4 14,058 1015 7.2 0.97 0.89 1.05 0.99 0.91 1.07
The ages and stages questionnaire (ASQ)
 Communication
  PA = 0 15,207 15 0.1 0.74 0.37 1.48 0.76 0.38 1.52
  Quartile 1 12,793 17 0.1 Ref Ref
  Quartile 2 12,050 10 0.1 0.63 0.29 1.38 0.62 0.28 1.36
  Quartile 3 13,536 16 0.1 0.91 0.46 1.80 0.90 0.46 1.78
  Quartile 4 12,860 7 0.1 0.43 0.18 1.04 0.45 0.18 1.08
Gross motor skills
PA = 0 15,212 902 5.9 1.04 0.95 1.14 1.05 0.95 1.15
Quartile 1 12,791 724 5.7 Ref Ref
Quartile 2 12,050 667 5.5 0.99 0.89 1.09 0.98 0.89 1.09
Quartile 3 13,533 700 5.2 0.93 0.84 1.03 0.94 0.85 1.04
Quartile 4 12,861 643 5.0 0.93 0.83 1.03 0.95 0.86 1.06
Fine motor skills
PA = 0 15,200 1022 6.7 1.16 1.06 1.27 1.14 1.04 1.25
Quartile 1 12,790 733 5.7 Ref Ref
Quartile 2 12,043 635 5.3 0.92 0.83 1.03 0.93 0.84 1.03
Quartile 3 13,533 694 5.1 0.91 0.82 1.01 0.92 0.83 1.01
Quartile 4 12,854 622 4.8 0.88 0.79 0.98 0.87 0.78 0.97
Problem-solving
PA = 0 15,182 922 6.1 1.15 1.05 1.27 1.14 1.03 1.25
Quartile 1 12,774 666 5.2 Ref Ref
Quartile 2 12,033 622 5.2 1.00 0.90 1.11 0.99 0.89 1.10
Quartile 3 13,521 648 4.8 0.94 0.84 1.04 0.94 0.85 1.04
Quartile 4 12,849 545 4.2 0.85 0.76 0.95 0.86 0.77 0.96
Personal–social characteristics
PA = 0 15,168 213 1.4 1.29 1.04 1.60 1.27 1.03 1.58
Quartile 1 12,764 138 1.1 Ref Ref
Quartile 2 12,014 131 1.1 1.01 0.80 1.29 1.03 0.81 1.31
Quartile 3 13,509 147 1.1 1.02 0.81 1.29 1.05 0.84 1.33
Quartile 4 12,830 132 1.0 0.99 0.78 1.25 0.98 0.77 1.25
Total (abnormal score for any 1 of the 5 domain)
PA = 0 15,214 2352 15.5 1.10 1.04 1.16 1.09 1.03 1.16
Quartile 1 12,798 1789 14.0 Ref Ref
Quartile 2 12,055 1601 13.3 0.96 0.90 1.02 0.96 0.90 1.02
Quartile 3 13,540 1738 12.8 0.93 0.88 0.99 0.95 0.89 1.01
Quartile 4 12,864 1517 11.8 0.88 0.82 0.94 0.89 0.84 0.95
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PA physical activity, CI confidence interval, RR risk ratio, Ref reference.

aAdjusted for maternal age at delivery, smoking habits, alcohol consumption, pre-pregnancy body mass index, gestational age at birth, parity, infertility treatment, infant sex, type of delivery, psychological distress at 1 year after delivery, doctor diagnosis of asthma and atopic dermatitis at 1-year-old, and feeding status.

Association of maternal PA before and during pregnancy with development in 1-year-old infants

Low levels of maternal PA both before and during pregnancy were associated with an increased risk of abnormal ASQ scores. Compared to the reference PA group before pregnancy, the group with the lowest levels of PA (PA = 0) had higher risk ratios of abnormal scores in the following domains of the ASQ: fine motor skills (RR = 1.15, 95% CI = 1.05–1.26), problem-solving (RR = 1.20, 95% CI = 1.09–1.33), and personal–social skills (RR = 1.29, 95% CI = 1.04–1.60) (Table 2).

Correspondingly, the risk ratios of abnormal scores for different domains of the ASQ were lower in the group with highest levels of PA (quartile 4) before pregnancy: fine motor skills (RR = 0.81, 95% CI = 0.73–0.90), problem-solving (RR = 0.86, 95% CI = 0.78–0.96), and overall skills (RR = 0.84, 95% CI = 0.79–0.90).

Similar associations were found in the analysis of PA during pregnancy (Table 3). Compared to the reference group for PA during pregnancy, the group with the lowest PA levels (PA = 0) showed higher risk ratios of abnormal scores in the following ASQ domains: fine motor skills (RR = 1.14, 95% CI = 1.04–1.25), problem-solving (RR = 1.14, 95% CI = 1.03–1.25), personal–social skills (RR = 1.27, 95% CI = 1.03–1.58), and overall skills (RR = 1.09, 95% CI = 1.03–1.16).

Conversely, in the group with the highest PA levels during pregnancy (quartile 4), the risk ratios of abnormal ASQ scores were lower in the following domains: fine motor skills (RR = 0.87, 95% CI = 0.78–0.97), problem-solving (RR = 0.86, 95% CI = 0.77–0.96), and overall skills (RR = 0.89, 95% CI = 0.84–0.95).

In other domains of the ASQ, including communication and gross motor skills, maternal PA both before and during pregnancy was not associated with significant risk ratios of abnormal scores.

The association between the risk ratios of abnormal ASQ scores and maternal PA levels, both before and during pregnancy, did not change in the subgroup analysis that excluded women with HDP and GDM (Table S2).

Discussion

In the present study, lower maternal PA levels before and during pregnancy increased the risk ratios of abnormal scores on the infants’ ASQ at 1 year of age. Higher maternal PA levels were associated with lower risk ratios of abnormal ASQ scores. Similarly, maternal PA levels before and during pregnancy were inversely associated with infant late bedtime at or after 22:00, as shown by the risk ratio. However, other sleep outcomes were not associated with maternal PA levels. This is the first study to show that maternal PA levels before pregnancy influence measures of development and concur with previous findings associated with PA during pregnancy. Higher PA levels during preconception may decrease the risk of developmental delay.

Regarding infant sleep problems, lower maternal PA levels before and during pregnancy were associated exclusively with late bedtime in 1-year-old infants. In this study, the proportion of infants who fell asleep after 22:00 was approximately 20%, which is a larger percentage than other sleep outcomes. Thus, a small but significant difference in late bedtime was detected. A high level of maternal activity during pregnancy has been reported to improve maternal sleep15,16. The sleep cycle develops from the fetal period17, and the association between maternal sleep during pregnancy and infants’ sleep has also been reported18,19. Therefore, maternal PA during pregnancy may affect infants’ sleep through maternal sleep. No other studies have addressed the direct association between maternal PA and infant sleep patterns. Further investigations are required to evaluate these associations.

This is the first study to show that maternal PA before pregnancy may influence infant developmental outcomes. Regarding PA during pregnancy, there have been many previous studies that reported an association between PA during pregnancy and language development20–22. The association between PA during pregnancy, motor function, and social skills remains inconclusive5,6. A recent RCT study reported a positive association between maternal exercise and infant neuromotor outcomes at 1- month-old23. Although there was a significant association between maternal PA and child development, it was also reported that the association became insignificant as the child matured21,24. Future studies should investigate the association between maternal PA before and during pregnancy and development in older children.

There are several hypotheses on how maternal PA before and during pregnancy affects infant neurodevelopment. The first hypothesis involves maternal inflammation, which affects fetal neurodevelopment in utero and may cause developmental disorders25. One study reported that exercise intervention in pregnant women reduced inflammatory cytokines26. Therefore, high maternal PA levels may protect fetal neurodevelopment from inflammation.

The second hypothesis is that maternal PA directly affects neurodevelopment in infants. In an experiment with mice and rats, exercise during pregnancy improved neurogenesis in the hippocampus, memory, and learning outcomes27–31. From this study, it can be inferred that for humans, PA during pregnancy may have a beneficial influence on fetal neurodevelopment.

The third hypothesis is that maternal activity may stimulate fetal sensory systems, such as vestibular function. A study of preterm infants reported that auditory, tactile, visual, and vestibular interventions increased nipple feeding and decreased the length of infant hospitalization32. As fetal vestibular function develops from early pregnancy33,34, maternal PA may stimulate the fetal vestibular system to positively affect neurodevelopment.

Perinatal complications, such as GDM, HDP, and perinatal depression, have negative effects on child neurodevelopment1,2,35,36. These complications are known risk factors of developmental disorders11. However, in our subgroup analysis, which excluded cases of HDP and GDM, an association between abnormalities in ASQ scores and maternal PA before and during pregnancy was found. This finding implies that HDP and GDM may not be the only complications associated with maternal PA before and during pregnancy.

This study has several limitations. First, this was an observational study, so there could be unmeasured confounding factors, such as parental life rhythm or sleep cycle. Second, maternal PA and infant outcomes (infant sleep problems and ASQ scores) were evaluated using a self-reported questionnaire, so there could be some bias. In particular, maternal PA before pregnancy was reported at recruitment in the first trimester of pregnancy. On the other hand, the strength of the present study was that it was based on national data. Additionally, this was the first study to focus on the association between maternal PA before pregnancy and infant development.

In conclusion, lower maternal PA before or during pregnancy was associated with negative effects on infant development and increased risk of late bedtimes in 1-year-old infants. In contrast, higher maternal PA before or during pregnancy may have positive effects on infant development and decrease the risk of late bedtimes in 1-year-old infants.

Methods

Research ethics

The study protocol was approved by the Ministry of the Environment’s Institutional Review Board on Epidemiological Studies (No. 100406001) and by the Ethics Committee of all participating institutions: the National Institute for Environmental Studies that leads the Japan Environment and Children’s Study (JECS), the National Center for Child Health and Development, Hokkaido University, Sapporo Medical University, Asahikawa Medical College, Japanese Red Cross Hokkaido College of Nursing, Tohoku University, Fukushima Medical University, Chiba University, Yokohama City University, University of Yamanashi, Shinshu University, University of Toyama, Nagoya City University, Kyoto University, Doshisha University, Osaka University, Osaka Medical Center and Research Institute for Maternal and Child Health, Hyogo College of Medicine, Tottori University, Kochi University, University of Occupational and Environmental Health, Kyushu University, Kumamoto University, University of Miyazaki, and University of Ryukyu. Written informed consent, which also included a follow-up study of children after birth, was obtained from all participants. All methods were performed in accordance with approved guidelines.

Study participants

The data used in this study were obtained from the JECS, an ongoing large-scale cohort study. The JECS was designed to follow children from the prenatal period to the age of 13 years. The detailed protocol of the study and the baseline profile of participants in the JECS have been previously reported previously37,38. The participants answered a questionnaire about lifestyle and behavior twice during pregnancy. The questionnaire completed at recruitment was referred to as M-T1, and the questionnaire completed later during mid- and late pregnancy was M-T2. The mean gestational weeks (SD) at the time of responding to M-T1 and M-T2 were 16.4 (8.0) and 27.9 (6.5) weeks, respectively. Participants also answered a questionnaire about their offspring one year after delivery (C-1y).

Between 2011 and 2014, 103,062 pregnant women were recruited from 15 regions throughout Japan (Fig. 1). Of these, we excluded 26,694 pregnancies due to the following reasons: previous participation in the study (n = 5647), multiple fetuses (n = 949), miscarriage or stillbirth (n = 3,676), congenital anomaly or disease at 1 month of age (n = 3553), missing information on maternal age at delivery (n = 7), delivery before 37 weeks or after 42 weeks of gestation (n = 4184), lack of information about maternal PA in the M-T1 and M-T2 (n = 1109), and no response to questions about children’s sleep and development at C-1y (n = 7569). The remaining 76,368 participants (74,971 with M-T1 data and 72,700 with M-T2 data) were included in the analysis.

Figure 1.

Figure 1

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Population flowchart. PA, physical activity; M-T1, questionnaire administered at recruitment; M-T2, questionnaire administered during mid- and late pregnancy; ASQ, Ages and Stages Questionnaire.

Exposure: maternal PA

We used the Japanese short version of the International Physical Activity Questionnaire (IPAQ) to evaluate maternal PA, for which test–retest reliability and criterion validity were reported elsewhere39,40. Participants reported their mean PA per week before pregnancy on the M-T1 questionnaire based on recall and their mean PA per week during pregnancy on the M-T2 questionnaire. We calculated PA in terms of metabolic equivalent of a task (MET), measured as the number of minutes per week (METs-min/week)39. PA, as defined in the IPAQ, includes all activities of daily life, such as work, housework, and leisure activities.

We divided the participants into five groups based on their level of PA before pregnancy. We also divided the participants into five groups based on their levels of PA during pregnancy. In each of the five groups, the “PA = 0” group consisted of participants whose PA was 0. The other participants were divided into four groups using PA quartile points. The groups were labeled Quartiles 1–4 in ascending order of PA. Quartile 1 referred to the group with the lowest PA levels among the four groups. Quartile 4 referred to the group with the highest PA levels. To visualize the effects when the amount of activity was very low, we defined the Quartile 1 groups as the reference groups for the purpose of statistical analysis instead of the PA = 0 groups.

Outcome 1: infant sleeping problems

One year after delivery, information on infant sleep habits was collected via parent-reported questionnaires (C-1y). The participants answered questions regarding their infant’s sleep time in the previous 24 h, in 30-min increments. They were also asked whether their children cried at night, and if so, the crying frequency (“rarely,” “1–3 times in a month,” “1–2 times in a week,” “3–4 times in a week,” “5 times in a week or more”) was reported. In this analysis, we focused on five points. First, we determined the number of nocturnal awakenings from maternal responses to infants’ sleeping periods. We defined ≥ 3 awakenings as too many because a previous study reported that the upper limit of the number of awakenings during the night was 2.5 for 1-year-old infants41. Second, we determined whether the infants awoke more than once and whether they stayed awake for more than 1 h during the night. If so, these were defined as unusual. Third, we analyzed the duration of nighttime sleep (20:00–07:59). We regarded less than 8 h of sleep as too short because past research reported that the mean duration of sleep for this age group was 8.3 h41. Fourth, we determined the infants’ bedtime. In this study, about 65% of 1-year-old infants slept later than 21:00, and about 20% slept later than 22:00. Therefore, we defined bedtime after 22:00 as too late. Fifth, we obtained information about crying at night in the past month. If the mother answered that her infant cried during the night, and the frequency of crying at night was more than five times per week, we defined the case as “crying at night”.

Outcome 2: infant development

We used the Japanese version of the Ages and Stages Questionnaire (ASQ), third edition, to evaluate infant development. The C-1y questionnaire included ASQ. ASQ captures developmental delay in five domains: communication, gross motor skills, fine motor skills, problem-solving, and personal–social characteristics. The answer to each question is one of the following: “yes,” “sometimes,” or “not yet.” The scores were 10, 5, and 0 points, respectively. Each ASQ domain was composed of six questions, and the total score ranged from 0 to 60. The cut-off point for each domain in the Japanese version was 2SD below the mean, and all the cut-off points were determined by age groups in a previous study42. The cut-off points at 1-year-old are as follows: communication, 4.53; gross motor skill, 9.43; fine motor skill, 25.47; problem solving, 15.37; and personal-social characteristics, 4.95. The outcomes were defined as whether the score was less than the cut-off point for each ASQ domain and whether the score was less than the cut-off point of any one of the five ASQ domains.

Covariates

Information on maternal age at delivery, pre-pregnancy body mass index (BMI), parity, gestational age at birth, infertility treatment, type of delivery, current history of hypertensive disorders of pregnancy and diabetes or gestational diabetes, infant birth weight, and infant sex were collected from medical records. Information about smoking habits, alcohol consumption, educational background, household income, maternal psychological distress at 1 year after delivery, doctor diagnosis of asthma and atopic dermatitis in children up to 1 year of age, and feeding status were collected via self-administered questionnaires. Maternal depression has been reported to affect infant development43. In the present study, we did not know whether the participants had a mental illness after delivery. Thus, maternal psychological distress was assessed using the Kessler 644,45 questionnaire at C-1y. In concordance with previous studies, participants with a score of five or more were categorized as having distress46.

Statistical analyses

We used a log-binominal regression model to explore the association of maternal PA with each outcome and to estimate the risk ratio (RR) of each outcome and the 95% confidence intervals (CIs). We initially adjusted for maternal age at delivery and then further adjusted for smoking habits (never smokers, ex-smokers who quit before pregnancy, smokers during early pregnancy), alcohol consumption (never drinkers, ex-drinkers who quit before pregnancy, drinkers during early pregnancy), pre-pregnancy BMI (< 18.5, 18.5–24.9, ≥ 25.0 kg/m2), parity (0, ≥ 1), infertility treatment (no ovulation stimulation/artificial insemination by sperm from husband, assisted reproductive technology), type of delivery (vaginal or cesarean section), gestational age at birth (37–38, 39–41 weeks), infant sex (boys, girls), psychological distress at 1 year after delivery (yes, no), doctor diagnosis of asthma and atopic dermatitis at 1 year of age, and feeding (breast milk, formula, both). The covariates to be added to the multivariate model were determined by referring to the previous literature as potential risk factors for developmental disorders11,47. Due to the large sample size in this study, we used the risk factors contained in the dataset in the multivariate model as covariates whenever possible. However, since there were many missing data on household income and educational background, we excluded them from the covariates of the multivariate model after confirming that the results did not change significantly even if they were included in the model. We did not complete the missing data. Thus, the multivariate analysis was limited to those participants that had all the covariate data.

We also performed a subgroup analysis excluding women with HDP and GDM to investigate the influence of these factors on infant development.

In this study, we used a fixed dataset “jecs-an-20180131,” which was released in March 2018. Stata version 15 (StataCorp LP, College Station, TX, USA) was used for all statistical analyses.

The statistical analyses of this study were conducted in a manner that was similar to that of our previous study48.

Supplementary Information

Supplementary Information. (49.6KB, docx)

Acknowledgements

We would like to express our gratitude to all the participants of this study and all individuals involved in data collection. This work was inspired by other works supported by the RIKEN Healthcare and Medical Data Platform Project and JSPS KAKENHI (Grant Nos.: JP16H01880, JP16K13072, JP18H00994, 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., 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.

Funding

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 Ministry of the Environment.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher's note

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

These authors contributed equally: Kazushige Nakahara and Takehiro Michikawa.

A list of authors and their affiliations appears at the end of the paper.

Contributor Information

Seiichi Morokuma, Email: morokuma@med.kyushu-u.ac.jp.

the Japan Environment and Children’s Study Group:

Michihiro Kamijima, Shin Yamazaki, Yukihiro Ohya, Reiko Kishi, Nobuo Yaegashi, Koichi Hashimoto, Chisato Mori, Shuichi Ito, Zentaro Yamagata, Hidekuni Inadera, Takeo Nakayama, Hiroyasu Iso, Masayuki Shima, Youichi Kurozawa, Narufumi Suganuma, and Takahiko Katoh

Supplementary Information

The online version contains supplementary material available at 10.1038/s41598-021-87612-1.

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