Mediation of pediatric atopic dermatitis in emotional and behavioral outcomes by sleep disturbance.

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Published in final edited form as: Ann Allergy Asthma Immunol. 2025 May 31;135(4):434–442. doi: 10.1016/j.anai.2025.05.026 Mediation of pediatric atopic dermatitis in emotional and behavioral outcomes by sleep disturbance Aaron Bao 1 , Patrick G Sockler 2 , Cyd K Eaton 1 , Sarah Radtke 1 , Adam P Spira 1, 3 , Joy Wan 1 Author information Article notes Copyright and License information 1 Johns Hopkins University School of Medicine, Baltimore, Maryland 2 Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 3 Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland ✉ Corresponding author: Joy Wan MD, MSCE, 200 N. Wolfe St., Suite 2107, Baltimore, Maryland, 21287, Fax: 410-614-9308, jwan7@jhmi.edu Issue date 2025 Oct. PMC Copyright notice PMCID: PMC12231109  NIHMSID: NIHMS2093740  PMID: 40456485 The publisher's version of this article is available at Ann Allergy Asthma Immunol Abstract Background: Atopic dermatitis (AD) is associated with increased risk of emotional and behavioral problems in children, but the mechanisms underlying this relationship are not fully understood. Objective: To evaluate sleep disturbance and sleep duration as potential mediators between AD and emotional/behavioral problems in children across childhood. Methods: We performed mediation analyses at three timepoints using data from the Avon Longitudinal Study of Parents and Children birth cohort in the United Kingdom. The exposure was child’s AD status, categorized as no AD, inactive AD, mild active AD, or moderate/severe active AD. Mediators were maternal-reported child sleep disturbances and total 24-hour sleep duration. Outcomes were emotional and behavioral problems assessed via the parent-reported Strengths and Difficulties Questionnaire (SDQ) and depressive symptoms via the Short Moods and Feelings Questionnaire (SMFQ). Analyses were adjusted for sociodemographic factors. Results: More active/severe AD was associated with greater sleep disturbance and higher levels of emotional/behavioral problems across all timepoints. Mediation models revealed significant direct effects of active AD on SDQ total difficulties. Indirect effects mediated by sleep duration were minimal (<1% of total effect), while those mediated by sleep disturbance were significant across AD severity strata for SDQ (6.5–26.7% of total effect) and SMFQ (10.9–14.0% of total effect). Bedtime refusal and early awakenings were most strongly associated with clinically-concerning SDQ scores. Conclusion: Sleep disturbance significantly mediates the association between AD and emotional/behavioral problems in children. Interventions targeting sleep may be one approach to reducing the psychological burden of AD in pediatric populations. Keywords: atopic dermatitis, sleep, psychology, eczema, pediatrics Introduction: Atopic dermatitis (AD) is a chronic inflammatory skin disease affecting up to 20% of children. AD has been associated with greater psychological comorbidities, including attention-deficit/hyperactivity disorder, anxiety disorder, and depression 1 , 2 , leading to poor quality of life and school absenteeism 3 , 4 . It has been postulated that sleep disturbances—present in up to two-thirds of individuals with AD 5 —may drive the disease-associated psychological burdens. The interrelationships among AD, sleep, and mental health have been described, with children with AD having elevated risks of both psychological disorders and sleep disturbances, which are themselves bidirectionally linked through biological and social factors 6 – 8 . However, the nature of the intersecting pathways among AD, sleep, and mental health has not been fully characterized, and few studies have explicitly examined sleep as a mediator of psychological outcomes in pediatric AD. Thus, we leveraged longitudinal data from a large UK birth cohort to test the hypothesis that sleep duration and disturbance mediate the relationship between AD and emotional and behavioral problems in childhood. Additionally, we explored whether specific sleep disturbances might differentially influence psychological symptoms. Delineating these pathways may inform preventive strategies and interventions to optimize mental health outcomes for the many children affected by AD worldwide. Methods: Participants We conducted a series of mediation analyses using data from the Avon Longitudinal Study of Parents and Children (ALSPAC), a birth cohort that enrolled 14,451 pregnant women from Avon, UK with expected delivery dates between 1991 and 1992, resulting in 13,988 children alive at 1 year of age 9 , 10 . The children and their families have since been continuously followed via questionnaires and clinic visits. Please note that the study website contains details of all the available data through a fully searchable data dictionary and variable search tool ( http://www.bristol.ac.uk/alspac/researchers/our-data ). Ethical approval for the study was obtained from the ALSPAC Ethics and Law Committee and the Local Research Ethics Committees. Exposures The exposure of interest was AD status, assessed using a maternal questionnaire administered approximately annually between 6 months and 8.5 years of age. AD was evaluated using the question “Has your child had a skin rash in the joints and creases of their body (e.g. behind the knees, elbows, under the arms) in the past 6–12 months?”, based on the validated International Study of Asthma and Allergies in Childhood and U.K. Working Party diagnostic criteria for AD 11 . Participants were considered to have AD if they had ≥2 reports of AD up to and including the timepoint being analyzed. At each timepoint, those reporting AD symptoms within the past year were classified as having ‘active’ AD, with severity further categorized as ‘mild’ or ‘moderate/severe’ based on caregiver report. Those with AD but no symptoms in the last year were classified as having ‘inactive’ AD. Mediators The mediators of interest were sleep duration and sleep disturbance, measured via repeated maternal surveys between 6 months and 9.5 years old. Sleep duration was the total number of hours slept in a 24-hour period, rounded to the nearest tenth. Sleep disturbance was evaluated by a questionnaire asking if: “their child regularly…refused to go to bed; …had difficulty going to sleep; …had nightmares; …continued to get up after being put to bed; …awoke in the night; …got up after only a few hours of sleep; …awoke very early”. Each question offered an ordinal response scale: (0) no; (1) yes, no worry; (2) yes, some worry; or (3) yes, much worry. The composite sleep disturbance score was defined as the sum of the response scores for all 7 questions, resulting in a continuous 21-point scale with higher scores indicating greater sleep disturbance concerns. Outcomes Emotion and behavior outcomes were assessed using the validated Strengths and Difficulties Questionnaire (SDQ) and Short Moods and Feeling Questionnaire (SMFQ) administered to parents. SDQ was assessed at 4, 8, and 10.5 years old. SMFQ was assessed once at 10.5 years old. The SDQ is a well-established screening questionnaire consisting of four 10-point subscores (emotion, conduct, hyperactivity/inattention, and peer relationships), resulting in a cumulative score ranging from 0 to 40 12 . Clinically concerning symptoms were defined using established score cutoffs of >16 for SDQ total difficulties, >3 for conduct, >4 for emotion, >3 for peer problems, and >6 for hyperactivity/inattention 13 . The SMFQ, which screens for depression, ranges in score from 0 to 26, with scores >8 indicating presence of depressive symptoms 14 . Statistical analysis Patient characteristics, including mediators, outcomes, and covariates, were compared across AD severity groups. Differences in continuous and binary variables were determined using Jonckheere-Terpstra or ANOVA and Cochran-Armitage or Chi-square tests, respectively. Separate mediation analyses were conducted at three timepoints, each defined by the temporal sequence of AD status, followed by sleep measures, followed by emotion and behavior outcomes. To ensure consistency, we selected timepoints for which the exposure-to-mediator and mediator-to-outcome durations were both <2 years. The three timepoints were designated as early (AD at 2.5 years of age, sleep at 3.5 years, SDQ at 4 years), middle (AD at 5.75 years of age, sleep at 6.75 years, SDQ at 8 years), and late (AD at 8.5 years of age, sleep at 9.5 years, SDQ at 11 years and SMFQ at 10.5 years) ( Figure 1A ). Figure 1: Study design and model. Open in a new tab a) Timing of assessment for exposure, mediator, and outcome variables used in the mediation analysis at each timepoint. B) Conceptual model of AD’s effects on emotion and behavior with mediation by sleep. Parallel mediation modeling, a method based on regression techniques, was utilized to characterize the effects of AD status on emotion and behavior via sleep duration and disturbance. Mediation analysis was performed using the PROCESS R-package (version 4.3.1) and adjusted for potential confounders defined a priori , including child sex, parental education, household crowding index, financial difficulties score, gestational age at birth, maternal age at birth, and baseline sleep measures (i.e., at time of exposure). The reference group for all mediation analyses was the ‘no AD’ group. The impact of AD status on SDQ total score, SDQ subscores or SMFQ was designated as the direct effect, whereas the impact of AD status on SDQ or SMFQ via sleep duration or disturbance were designated as the indirect effects ( Figure 1B ). Direct and indirect effects were represented by B-coefficients, and the total effect was defined as the sum of both coefficients. The B-coefficient represents the magnitude of change in the outcome variable (SDQ or SMFQ score) associated with each category of AD severity compared to no AD; a positive B-coefficient indicates higher psychological symptom scores in children with a given AD severity level compared to children without AD, either directly or indirectly through sleep measures. The proportion of mediation was calculated by dividing the indirect effect coefficient by the total effect coefficient. Finally, multivariable logistic regression analysis, adjusted for sociodemographic characteristics and AD status, was conducted to explore the odds of clinically concerning total SDQ scores with respect to individual sleep disturbance components, dichotomized as either absent or present regardless of degree of concern. All statistical analyses were performed using R (version 4.2.3). Statistical significance was assumed when p <.05. This study was approved by the Johns Hopkins Institutional Review Board. Results: Participant characteristics Our analysis included 8,204 early-, 6,002 middle-, and 5,618 late-timepoint participants with complete exposure, mediator, and outcome data ( Table 1 ). The prevalence of moderate/severe AD was highest at the early (7.8%) compared to middle (5.6%) and late (4.5%) timepoints. Conversely, the late timepoint had the highest proportion of inactive AD (23.4%) compared to middle (19.5%) and early (6.4%) timepoints. Table 1: Characteristics of study population with respect to AD activity and severity at early, middle, and late timepoints. Characteristic, by timepoint of assessments AD activity and severity No AD Inactive AD Mild AD Moderate/Severe AD p a Exposure Participants in each AD group, n (%) Early (n = 8204) 6002 (73.2%) 523 (6.4%) 1042 (12.7%) 637 (7.8%) N/A Middle (n = 6002) 3601 (59.9%) 1169 (19.5%) 894 (14.9%) 338 (5.6%) N/A Late (n = 5618) 3229 (57.4%) 1318 (23.4%) 816 (14.5%) 255 (4.5%) N/A Mediators Sleep disturbance score (0–21), mean (SD) Early 3.64 (3.06) 3.71 (2.81) 3.87 (3.15) 4.47 (3.15) <0.001 Middle 3.82 (2.55) 4.01 (2.49) 4.03 (2.62) 4.36 (2.67) <0.001 Late 2.14 (2.18) 2.24 (2.19) 2.24 (2.17) 2.61 (2.49) 0.002 Hours slept in 24-hour period, mean (SD) Early 11.50 (0.91) 11.46 (0.84) 11.46 (0.87) 11.49 (0.94) 0.95 Middle 10.67 (0.85) 10.67 (0.83) 10.67 (0.83) 10.67 (0.76) 0.64 Late 9.93 (0.84) 9.92 (0.83) 9.95 (0.82) 9.92 (0.78) 0.65 Outcome SDQ total score (0–40), mean (SD) Early 8.72 (4.57) 9.35 (4.50) 9.01 (4.54) 9.53 (4.74) <0.001 Middle 7.52 (5.04) 7.68 (4.99) 7.68 (4.86) 8.44 (5.42) 0.002 Late 6.27 (4.85) 6.36 (4.85) 6.46 (4.88) 7.47 (5.19) 0.003 SDQ clinical concern (score >16), n (%) Early 400 (6.68%) 42 (8.43%) 75 (7.38%) 56 (9.09%) 0.03 Middle 263 (6.96%) 83 (6.89%) 63 (6.75%) 33 (9.94%) 0.30 Late 172 (4.79%) 70 (4.92%) 45 (5.15%) 17 (6.20%) 0.37 SMFQ total score (0–26), mean (SD) Late b 3.88 (3.38) 3.97 (3.45) 4.03 (3.46) 4.65 (3.89) 0.007 SMFQ clinical concern (score >8), n (%) Late 334 (10.18%) 135 (10.84%) 90 (11.61%) 44 (18.72%) 0.004 Covariates Female sex, n (%) Early 2897 (48.6%) 257 (49.2%) 516 (49.3%) 279 (43.1%) 0.12 Middle 1727 (48.0%) 579 (49.5%) 475 (53.1%) 164 (48.5%) 0.05 Late 1546 (47.8%) 619 (46.2%) 489 (59.9%) 138 (54.1%) <0.001 Gestational age at birth, months, mean (SD) Early 39.37 (1.95) 39.67 (1.57) 39.57 (1.77) 39.51 (1.70) <0.001 Middle 39.42 (1.88) 39.59 (1.60) 39.49 (1.89) 39.51 (1.64) 0.006 Late 39.41 (1.91) 39.50 (1.76) 39.48 (1.90) 39.67 (1.71) <0.001 Maternal age at birth, years, mean (SD) Early 28.52 (4.79) 28.82 (4.61) 28.77 (4.56) 28.49 (4.58) 0.29 Middle 28.80 (4.74) 28.79 (4.54) 29.19 (4.36) 28.62 (4.55) 0.26 Late 28.88 (4.75) 28.93 (4.50) 29.36 (4.30) 28.53 (4.39) 0.21 Maternal FDS c , mean (SD) Early 8.72 (4.57) 9.35 (4.50) 9.01 (4.54) 9.53 (4.74) 0.46 Middle 7.52 (5.04) 7.68 (4.99) 7.68 (4.86) 8.44 (5.42) 0.41 Late 6.27 (4.85) 6.36 (4.85) 6.46 (4.88) 7.47 (5.19) 0.83 Crowding index >0.75 d , n (%) Early 1759 (29.4%) 142 (27.2%) 234 (22.4%) 158 (24.8%) 0.003 Middle 1166 (32.4%) 324 (27.7%) 207 (23.1%) 86 (25.4%) <0.001 Late 984 (30.5%) 354 (26.8%) 191 (23.4%) 66 (25.8%) 0.002 Parent educational attainment of A-level or university equivalent, n (%) Early 3287 (54.8%) 248 (47.4%) 439 (42.1%) 300 (47.8%) <0.001 Middle 2207 (61.2%) 604 (51.6%) 442 (49.5%) 165 (48.8%) <0.001 Late 1903 (58.9%) 653 (49.5%) 397 (48.7%) 145 (56.9%) <0.001 Open in a new tab Abbreviations: AD, atopic dermatitis; FDS, financial difficulty score; SD, standard deviation; SDQ, Strengths and Difficulties Questionnaire; SMFQ, Short Moods and Feelings Questionnaire a Continuous variables were compared using the Jonckheere-Terpstra test (for mediators and outcomes) or ANOVA test (for covariates). Binary variables were compared using the Cochran-Armitage test (for mediators and outcomes) or Chi-square test (for covariates). N/A was used to denote that statistical tests were not performed for exposures. b SMFQ data was only available at the late timepoint. c Financial difficulty score (FDS) is a 9-point scale assessing mother’s financial ability to afford lodging, food, heating, clothing, and items for the child, recorded during gestational period. Higher scores correspond to greater financial difficulty. d Crowding index is calculated by dividing the number of people living in the home inhabited by the mother and child by the number of rooms (excluding bathrooms), recorded during gestational period. Crowding index >0.75 is used to define household crowding. Sleep disturbance was associated with greater AD activity/severity across all timepoints. In contrast, sleep duration did not differ significantly by AD activity/severity, and average number of hours slept was highest at the early timepoint (mean 11.5 [SD 0.92] hours), compared to middle (10.7 [0.85]) and late (9.92 [0.84]) timepoints ( p <0.001) ( Table 1 ). More active/severe AD was associated with higher SDQ total difficulties and SMFQ scores, with the moderate/severe AD group having the highest prevalence of clinically concerning scores ( Table 1 ). The prevalence of clinically concerning SDQ subscores varied across subscales ( Table 2 ). SDQ emotion subscores were significantly higher with more active/severe AD ( p <0.001 for all timepoints) but were generally lower in early versus later timepoints. Higher conduct and hyperactivity/inattention subcores were observed, and also correlated with more active/severe AD, at early timepoints, while peer problems subscores did not differ by AD activity/severity at any timepoint. Table 2. SDQ subscale scores by AD activity and severity at early, middle, and late timepoints of assessment. SDQ subscale, by timepoint of assessment AD activity and severity No AD Inactive AD Mild AD Moderate/Severe AD p a Conduct Total score (0–10), mean (SD) Early 1.92 (1.41) 2.14 (1.45) 1.95 (1.39) 2.07 (1.47) 0.001 Middle 1.47 (1.44) 1.49 (1.43) 1.45 (1.44) 1.75 (1.64) 0.12 Late 1.18 (1.41) 1.18 (1.38) 1.23 (1.44) 1.26 (1.44) 0.11 Clinical concern (score >3), n (%) Early 801 (13.3%) 90 (17.2%) 149 (14.3%) 104 (16.3%) 0.01 Middle 367 (10.2%) 129 (11.0%) 88 (9.8%) 44 (13.0%) 0.22 Late 262 (8.1%) 104 (7.9%) 71 (8.7%) 23 (9.0%) 0.34 Emotion Total score (0–10), mean (SD) Early 1.40 (1.48) 1.55 (1.56) 1.52 (1.53) 1.69 (1.64) <0.001 Middle 1.59 (1.76) 1.72 (1.84) 1.77 (1.87) 1.96 (2.05) <0.001 Late 1.37 (1.67) 1.49 (1.80) 1.56 (1.75) 1.93 (2.02) <0.001 Clinical concern (score >4), n (%) Early 265 (4.4%) 30 (5.7%) 52 (5.0%) 46 (7.2%) 0.002 Middle 318 (8.8%) 124 (10.6%) 95 (10.6%) 48 (14.2%) 0.003 Late 232 (7.2%) 113 (8.6%) 67 (8.2%) 34 (13.3%) 0.001 Hyperactivity/inattention Total score (0–10), mean (SD) Early 3.91 (2.32) 4.17 (2.32) 4.02 (2.29) 4.17 (2.44) 0.005 Middle 3.26 (2.45) 3.32 (2.39) 3.33 (2.44) 3.58 (2.56) 0.02 Late 2.77 (2.25) 2.70 (2.16) 2.67 (2.10) 3.13 (2.44) 0.34 Clinical concern (score >6), n (%) Early 872 (14.5%) 88 (16.8%) 157 (15.1%) 126 (20.1%) 0.001 Middle 446 (12.4%) 130 (11.1%) 113 (12.6%) 50 (14.8%) 0.32 Late 268 (8.3%) 91 (6.9%) 56 (6.9%) 31 (12.2%) 0.74 Peer problems Total score (0–10), mean (SD) Early 1.53 (1.50) 1.48 (1.41) 1.52 (1.50) 1.57 (1.56) 0.50 Middle 1.31 (1.54) 1.24 (1.48) 1.25 (1.49) 1.31 (1.51) 0.83 Late 1.10 (1.52) 1.02 (1.50) 1.17 (1.62) 1.27 (1.67) 0.42 Clinical concern (score >3), n (%) Early 679 (11.3%) 55 (10.5%) 116 (11.1%) 88 (13.8%) 0.16 Middle 381 (10.6%) 104 (8.9%) 93 (10.4%) 32 (9.5%) 0.56 Late 311 (9.6%) 113 (8.6%) 92 (11.3%) 30 (11.8%) 0.10 Open in a new tab Abbreviations: AD, atopic dermatitis; SDQ, Strengths and Difficulties Questionnaire. a Continuous variables compared using Jonckheere-Terpstra test and binary variables compared using Cochran-Armitage test. Mediation of AD on SDQ by sleep Across all timepoints, active AD had significant direct effects on SDQ total difficulties relative to no AD (B-coefficients for mild AD: early 0.36 [95% CI 0.07–0.65]; middle 0.38 [0.02–0.75]; late 0.37 [0.03–0.74]; moderate/severe AD: early 0.48 [0.12–0.85]; middle 0.57 [0.02–1.13]; late 0.71 [0.08–1.32]) ( Table 3 ). Inactive AD exhibited a significant direct effect only at the early timepoint (0.71 [0.32–1.10]). Table 3. Analysis of sleep disturbance and duration as mediators between AD activity and severity on SDQ and SMFQ total scores at early, middle, and late timepoints [ref: no AD]. All analyses were adjusted for sociodemographic characteristics including sex, gestational age and maternal age at child’s birth, parental education, household crowding index, financial difficulty score, and baseline sleep duration and disturbance. Pathway AD activity/severity B-Coeff SE 95% Confidence Interval SDQ Early Indirect effect (sleep disturbance) Inactive 0.049 0.023 0.002 – 0.104 Mild 0.078 0.027 0.024 – 0.132 Moderate/severe 0.144 0.039 0.072 – 0.225 Indirect effect (sleep duration) Inactive 0.008 0.012 −0.014 – 0.033 Mild 0.009 0.009 −0.008 – 0.028 Moderate/severe 0.009 0.012 −0.014 – 0.034 Direct effect by AD Inactive 0.707 0.200 0.315 – 1.100 Mild 0.358 0.149 0.066 – 0.650 Moderate/severe 0.482 0.187 0.116 – 0.847 SDQ Middle Indirect effect (sleep disturbance) Inactive 0.054 0.026 0.002 – 0.103 Mild 0.072 0.030 0.012 – 0.134 Moderate/severe 0.114 0.050 0.014 – 0.216 Indirect effect (sleep duration) Inactive 0.005 0.011 −0.020 – 0.026 Mild 0.008 0.009 −0.010 – 0.028 Moderate/severe 0.007 0.012 −0.014 – 0.034 Direct effect by AD Inactive 0.209 0.166 −0.115 – 0.525 Mild 0.379 0.182 0.017 – 0.746 Moderate/severe 0.568 0.279 0.024 – 1.132 SDQ Late Indirect effect (sleep disturbance) Inactive 0.072 0.026 0.021 – 0.123 Mild 0.096 0.043 0.013 – 0.187 Moderate/severe 0.161 0.064 0.032 – 0.297 Indirect effect (sleep duration) Inactive 0.000 0.003 −0.008 – 0.007 Mild 0.000 0.003 −0.007 – 0.006 Moderate/severe 0.000 0.005 −0.011 – 0.010 Direct effect by AD Inactive 0.198 0.157 −0.119 – 0.495 Mild 0.369 0.180 0.033 – 0.735 Moderate/severe 0.707 0.317 0.077 – 1.318 SMFQ Late Indirect effect (sleep disturbance) Inactive 0.022 0.011 0.001 – 0.044 Mild 0.049 0.022 0.006 – 0.096 Moderate/severe 0.061 0.025 0.010 – 0.112 Indirect effect (sleep duration) Inactive −0.001 0.003 −0.008 – 0.005 Mild 0.000 0.003 −0.007 – 0.005 Moderate/severe −0.001 0.006 −0.015 – 0.009 Direct effect by AD Inactive 0.155 0.122 −0.095 – 0.375 Mild 0.302 0.133 0.041 – 0.562 Moderate/severe 0.498 0.235 0.034 – 0.961 Open in a new tab Abbreviations: AD, atopic dermatitis; SDQ, Strengths and Difficulties Questionnaire; SMFQ, Short Moods and Feelings Questionnaire. Estimates with p<0.05 shown in bold. The indirect effect of AD on SDQ total difficulties mediated through sleep duration was minimal (<1% of total effect) across all timepoints, whereas the indirect effect mediated through sleep disturbance was significant for inactive AD (early 0.05 [0.002–0.10]; middle 0.05 [0.002–0.103]; late 0.07 [0.02–0.12]), mild AD (early 0.08 [0.02–0.13]; middle 0.07 [0.01–0.13]; late 0.10 [0.01–0.19]), and moderate/severe AD (early 0.14 [0.07–0.23]; middle 0.11 [0.01–0.22]; late 0.16 [0.03–0.30]) across all timepoints ( Table 3 ). The proportion of total effect mediated through sleep disturbance ranged from 6.5–26.7% for inactive AD, 16.0–20.6% for mild AD, and 16.7–23.0% for moderate/severe AD ( Figure 2 ). Figure 2: Effects of AD activity and severity on SDQ with proportions accounted for indirectly by sleep (reference: no AD). Open in a new tab Indirect effect is comprised of both sleep duration and disturbance. Because the indirect effect through sleep duration is <1% across all results, only one bar (lighter gray), representing the indirect effect through sleep disturbance, is shown. Analyses adjusted for sociodemographic characteristics and baseline sleep measures. For those with moderate/severe AD, sleep disturbance exhibited significant mediating effects across all SDQ subscores at most timepoints, with the proportion of total effect mediated through sleep disturbance ranging 11.7–16.5% for emotional symptoms, 8.2–42.3% for conduct problems, 14.7–26.9% for hyperactivity/inattention, and 16.2–49.8% for peer problems ( p <0.05 for all, Table 4 ). The indirect effect mediated through sleep disturbance was most consistently statistically significant for emotional symptoms, followed by hyperactivity/inattention and conduct problems, with the smallest effects observed for peer problems ( Table 4 ). Table 4: Effects of AD activity and severity on SDQ subscale scores with proportions of total effect accounted for indirectly by sleep disturbance. All analyses were adjusted for sociodemographic characteristics including sex, gestational age and maternal age at child’s birth, parental education, household crowding index, financial difficulty score, and baseline sleep duration and disturbance. SDQ subscale Direct and indirect effects of AD on SDQ scores mediated through sleep disturbance [ref: no AD] a Early timepoint Middle timepoint Late timepoint Direct effect by AD Indirect effect through sleep Proportion of indirect to total effect Direct effect by AD Indirect effect through sleep Proportion of indirect to total effect Direct effect by AD Indirect effect through sleep Proportion of indirect to total effect Emotion Inactive AD 0.1427 0.0034 2.3% 0.0672 0.0181 21.2% 0.1385 0.0156 10.1% Mild AD 0.1527 0.0158 9.4% 0.1279 0.0211 14.2% 0.1632 0.0187 10.3% Moderate/severe AD 0.2502 0.0332 11.7% 0.1697 0.0308 15.4% 0.4652 0.0918 16.5% Conduct Inactive AD 0.2618 0.0043 1.6% 0.0039 0.0070 64.3% 0.0270 0.0091 25.3% Mild AD 0.0417 0.0180 30.1% −0.0002 0.0093 N/A 0.0738 0.0124 14.4% Moderate/severe AD 0.1005 0.0348 25.7% 0.1868 0.0167 8.2% 0.0334 0.0245 42.3% Hyperactivity/inattention Inactive AD 0.3154 0.0056 1.7% 0.0182 0.0080 30.4% −0.0035 0.0134 N/A Mild AD 0.1937 0.0248 11.3% 0.1599 0.0206 11.4% 0.0716 0.0183 20.4% Moderate/severe AD 0.2257 0.0533 19.1% 0.2259 0.0389 14.7% 0.4227 0.1558 26.9% Peer problems Inactive AD −0.0286 0.0050 N/A −0.0389 0.0044 N/A −0.0522 0.0079 N/A Mild AD 0.0413 0.0115 21.8% −0.0789 0.0062 N/A 0.0542 0.0112 17.1% Moderate/severe AD 0.0238 0.0236 49.8% −0.0357 0.0109 N/A 0.1212 0.0235 16.2% Open in a new tab Abbreviations: AD, atopic dermatitis; SDQ, Strengths and Difficulties Questionnaire; SMFQ, Short Moods and Feelings Questionnaire. Estimates with p<0.05 shown in bold. a N/A is shown for the proportion of indirect to total effect when the direct and indirect effects had opposite directionality. Mediation of AD on SMFQ by sleep SMFQ was administered only at the late timepoint. There was a significant direct effect of mild AD (B 0.30, 95% CI [0.04, 0.56]) and moderate/severe AD (0.50 [0.03, 0.96]) on depressive symptoms, but no major direct effects from inactive AD (0.16 [−0.10, 0.38]), relative to no AD ( Table 3 ). Sleep duration minimally mediated the effect of AD on SMFQ total score (<1% of total effect), whereas sleep disturbance mediated the effects for inactive AD (B 0.02, 95% CI [0.001, 0.04]), mild AD (0.05 [0.01, 0.10]), and moderate/severe AD (0.06 [0.01, 0.11]) (all p<0.05). The proportion of AD’s total effect on SMFQ mediated through sleep disturbance ranged 10.9%−14.0% across different AD activity/severity strata ( Figure 3 ). Figure 3: Effects of AD activity and severity on SMFQ with proportions accounted for indirectly by sleep (reference: no AD). Open in a new tab Indirect effect is comprised of both sleep disturbance and duration. Because the indirect effect through sleep duration is <1% across all results, only one bar (lighter gray), representing the indirect effect through sleep disturbance, is shown. Analyses adjusted for sociodemographic characteristics and baseline sleep measures. Association of specific sleep disturbance measures with emotional or behavioral concerns In multivariable analyses, several sleep disturbance concerns were significantly associated with clinically concerning SDQ total scores. At the early timepoint, refusing to go to bed was associated with a 65% greater odds of clinically concerning scores (OR 1.65 [95% CI 1.32–2.07]) and difficulty falling asleep with a 45% greater odds of clinically concerning scores (1.45 [1.17–1.80]). At later timepoints, the strongest predictors of concerning scores were getting up after being put to bed (middle: 1.92 [1.51–2.47], late: 1.85 [1.35–2.55]) and refusing to go to bed (middle: 1.44 [1.14–1.83], late: 1.74 [1.29–2.37]). Refusing to go to bed and waking very early were consistently associated with concerning SDQ scores across all timepoints, whereas nightmares and getting up after being put to bed were primarily significant at later timepoints ( Table 5 ). Table 5: Odds of clinically concerning SDQ scores with respect to specific sleep disturbance measures. Multivariable models were adjusted for AD status and sociodemographic characteristics including sex, gestational age and maternal age at child’s birth, parental education, household crowding index, and financial difficulty score. Timepoint of sleep assessment Sleep disturbance measure Early (3.5 years old) Middle (6.75 years old) Late (9.5 years old) In the past year, has your child regularly… % [n] answering yes OR (95% CI) for SDQ clinical concern % [n] answering yes OR (95% CI) for SDQ clinical concern % [n] answering yes OR (95% CI) for SDQ clinical concern Refused to go to bed 43.8% (4379) 1.65 (1.32–2.07) 51.4% (4341) 1.44 (1.14–1.83) 33.7% (2723) 1.74 (1.29–2.37) Continued to get up after being put to bed 36.8% (3676) 1.13 (0.92–1.41) 38.8% (3265) 1.92 (1.51–2.47) 22.2% (1789) 1.85 (1.35–2.55) Gotten up after only a few hours of sleep 17.3% (1724) 1.21 (0.96–1.52) 12.3% (1033) 1.59 (1.19–2.11) 6.5% (525) 0.87 (0.53–1.40) Woken very early 54.9% (5479) 1.37 (1.11–1.70) 53.2% (4472) 1.38 (1.09–1.77) 36.6% (2946) 1.43 (1.07–1.92) Woken in the night 72.5% (7245) 1.20 (0.92–1.59) 69.2% (5795) 0.95 (0.72–1.26) 13.5% (1045) a 1.59 (1.10–2.25) Had difficulty falling sleep 37.3% (3723) 1.45 (1.17–1.80) 63.0% (5299) 1.19 (0.90–1.58) 52.4% (4226) 1.21 (0.87–1.69) Had nightmares 32.8% (3279) 1.13 (0.93–1.39) 49.5% (4130) 1.35 (1.06–1.75) 29.3% (2328) 1.69 (1.26–2.25) Open in a new tab Abbreviations: OR, odds ratio; CI, confidence interval. Estimates with p<0.05 shown in bold. a This specific data variable was missing from the original ALSPAC database due to an error in the original questionnaire administered by the ALSPAC team. A proxy continuous variable asking for “number of awakenings in the night” was used instead, with an answer ≥1 representing the presence of the “woken in the night” sleep disturbance measure. Discussion: Our findings suggest that sleep disturbance, more so than sleep duration, partially mediates the relationship between AD and emotional and behavioral problems across varying degrees of AD activity/severity and across multiple timepoints in childhood. We also identified specific sleep disturbances, most consistently bedtime refusal and early morning awakenings, that may contribute to the association between sleep and emotional/behavioral concerns in children with AD. Childhood AD is associated with a greater risk of both internalizing (e.g., anxiety and depression) 1 and externalizing disorders (e.g., ADHD and conduct issues) 2 . Consistent with prior literature, we observed direct associations between AD activity/severity and clinically concerning behavioral and emotional symptoms, with stronger and more consistent direct effects of moderate/severe AD on internalizing symptoms (e.g., SDQ emotion and SMFQ) and externalizing symptoms (e.g., SDQ hyperactivity/inattention). Sleep disturbances frequently co-occur with AD and are reported in up to two-thirds of children with AD, with more severe AD correlating with poorer sleep 6 , 15 . Proposed mechanisms implicate inflammatory neuronal sensitization and central nervous system dysregulation leading to poorer sleep, including lower sleep efficiency and less REM sleep 16 . Sleep impairments may persist even during AD remission, suggesting that active cutaneous symptoms are not the only drivers of these associations 17 . The nature of AD’s relationship with sleep duration versus sleep disturbance may also differ, with previous studies similarly indicating weaker associations of AD with sleep duration than with sleep quality or disturbance 18 , 19 . Finally, it is known that poor sleep is bidirectionally linked to adverse mental health outcomes among youth. Early childhood sleep problems predict future depression and anxiety disorders as well as ADHD 7 , 8 . Conversely, pre-existing psychiatric conditions also precipitate sleep disturbances, such as frequent awakenings, lighter sleep, and increased wakefulness 20 . Specific sleep disturbances may also differentially affect mental health 21 . For example, parasomnias are associated with a greater risk of subsequent externalizing, but not internalizing, behaviors 22 . While prior studies have documented independent associations of AD with both mental health problems and sleep disturbances 22 – 25 , few have examined sleep as a mediator of poor mental health in AD. One cross-sectional study found associations between AD and ADHD among children with sleep disturbances but not in those without 26 . Similarly, another small study of 77 children with AD found that sleep disruption mediated AD’s effects on symptoms of ADHD and oppositional defiant disorder 27 . Our study also extends prior findings in ALSPAC by systematically evaluating the mediating role of sleep across three developmental timepoints and for different types of emotional and behavioral problems. 1 Furthermore, our study’s three-timepoint design allowed us to examine whether relationships remained stable or evolved throughout development. Consistent with documented developmental sleep changes, average sleep disturbance improved and sleep duration decreased at older ages 28 , 29 . However, while risk for mental health disorders typically increases as children age 30 , rates of concerning emotional and behavioral symptoms generally decreased with age in our cohort, a finding which may be in part due to parental report. Despite these temporal fluctuations, the direct and indirect effects of AD on mental health were largely consistent across the timepoints we examined, suggesting that sleep disturbance is a relevant mediator independent of age. Our findings indicate that disturbed sleep may be one mechanism through which AD impairs mental health and thus serves as a targetable factor to reduce psychological morbidity in pediatric AD. While sleep disturbance showed partial mediating effects across all SDQ subscores for those with moderate/severe AD, the proportion of mediation by sleep varied, ranging from 8.2% for conduct problems to nearly 50% for peer problems in some age groups. This pattern of differential mediation across psychological domains has not been previously examined in AD and suggests that sleep may be particularly relevant for certain aspects of mental health in pediatric AD. Clinicians caring for patients with AD should consider screening for and addressing sleep disturbances to mitigate their potential negative mental health impacts. Emerging data suggest that treating AD may have ancillary benefits for sleep. A small prospective cohort study found topical corticosteroids improved parent-reported sleep quality in children, albeit without changes in objectively-measured sleep duration 31 . Similarly, dupilumab and tralokinumab, biologic agents targeting type-2 inflammatory pathways implicated in AD pathogenesis, have been associated with improvements in subjective sleep quality and measures of anxiety and depression 32 , 33 . Interventions targeting maladaptive sleep habits, such as cognitive behavioral therapy for insomnia or graduated extinction techniques for bedtime refusal, have also been shown to reduce sleep onset latency and awakenings after sleep onset and to improve global sleep quality ratings 34 , 35 . One randomized controlled trial also demonstrated that oral melatonin improved both AD severity and sleep onset latency in children and adolescents, though melatonin’s effects on other aspects of sleep are mixed 36 , 37 . Ultimately, multidisciplinary approaches involving dermatologists, sleep specialists, and mental health providers may be particularly beneficial for children with concurrent AD, sleep disturbances, and emotional or behavioral concerns. While sleep may be a mediator of mental health in AD, it is only a partial mediator and other contributing factors and mediators should still be considered 38 . For example, children with visible dermatologic conditions frequently experience psychosocial stressors such as stigmatization, bullying, and isolation that adversely impact psychological well-being 39 . Chronic systemic antihistamine use and parenting factors such as maternal stress may also contribute 40 – 42 . Thus, further research to identify other mechanistic factors is needed. Additionally, a multi-pronged approach addressing biologic, behavioral, and environmental factors may be necessary to optimize mental health in children with AD. Limitations Several limitations should be discussed. While we examined mediation at three childhood timepoints, each analysis was independently conducted, thus precluding evaluation of how AD and sleep disturbances at earlier timepoints might influence later outcomes. The one-year time lapses between exposure, mediator, and outcome variables may also confer some loss in model specificity given the dynamic nature of AD and sleep. Due to the longitudinal nature of the ALSPAC cohort, potential selection bias may have been introduced by participant attrition over time. Additionally, the study data was collected in the 1990s and early 2000s. While the biological mechanisms underlying the relationships between AD, sleep, and mental health are likely consistent today, AD management approaches have evolved since, making our findings potentially less generalizable to now. However, the mediation pathways identified in this study likely remain valid and relevant to contemporary populations, given that recent studies continue to document associations between AD, sleep disturbances, and psychological outcomes 1 , 22 – 25 . Parent-reported data on AD and sleep may lead to misclassification bias. While AD assessments mirrored validated diagnostic criteria and AD prevalence in ALSPAC aligned with other UK population-based estimates 19 , there were no objective measures of AD severity. Additionally, the sleep disturbance composite scale has not been formally validated; however, parental sleep reports often correlate with objective sleep measures, 43 and the sleep survey administered in ALSPAC included questions analogous to those in the validated Children’s Sleep Habits Questionnaire 44 . Lastly, while we adjusted for multiple confounders in the analysis, other variables of potential importance, such as self-efficacy of the child, parental sleep and mental health, and select comorbidities (e.g., allergic disorders or sleep apnea), were not assessed. Conclusion: Our findings suggest poor sleep as a potentially important modifiable risk factor that may partially mediate the adverse effects of AD on emotion and behavior in children. Notably, our study extended prior findings by examining multiple developmental periods and psychological domains as well as identifying specific sleep disturbance components – particularly bedtime refusal and early morning awakenings – that contribute most significantly to the AD-mental health relationship. While sleep disturbance appeared to be a stronger partial mediator than sleep duration, future longitudinal studies with objective measures of sleep are still needed to further dissect the short-term and long-term effects of sleep on psychological outcomes among children with AD. Nevertheless, attention to sleep in pediatric AD care remains important, and sleep-focused interventions should be evaluated as a potential strategy for reducing the psychological burden of AD in children. Funding/Support: The study was supported by a grant from the U.S. National Institutes of Health K23AR077629 (J.W.). The UK Medical Research Council and Wellcome (Grant ref: 217065/Z/19/Z) and the University of Bristol provide core support for ALSPAC. A comprehensive list of grants funding is available on the ALSPAC website ( http://www.bristol.ac.uk/alspac/external/documents/grant-acknowledgements.pdf ). The funding sources played no role in the design of the study, the collection, analysis and interpretation of data, and the writing of the manuscript. Conflicts Of Interest Disclosures: J.W. has received research and fellowship funding (paid to Johns Hopkins) from Pfizer and has served as an advisor to Janssen and Sun Pharmaceuticals (DMC), receiving honoraria. A.S. received payment for serving as a consultant for Merck, received honoraria from Springer Nature Switzerland AG for guest editing special issues of Current Sleep Medicine Reports, and is a paid consultant to Sequoia Neurovitality, BellSant, Inc., and Amissa, Inc. All other authors have no conflicts of interest to report. 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