Preliminary Exploration into the Impact of Mistimed Expressed Breast Milk Feeding on Infant Sleep Outcomes,Compared to Other Feeding Patterns

Abstract

Background and Objective:

The presence and fluctuation of melatonin in breast milk during the night and day may be providing sleep timing information to infants, thereby supporting/enabling the development of their own circadian cycle. If this is the case, then it is important that infants consume breast milk according to the time of day it is produced. However, breast milk is not always consumed at the “right” time. The aim of this study was to investigate whether consuming mistimed expressed breast milk impacts infant sleep compared with other feeding types.

Methods:

A total of 329 mothers completed an online anonymous survey. Mothers were grouped into one of five groups; direct breastfed only, formula only, express mistimed, express-timed, and combined breastfed/formula fed.

Results:

Cross-sectional analysis showed mistimed expressed breast milk was significantly associated with delayed sleep onset of the infant (p < 0.001), but direct breastfed infants had significantly more awakenings at night (p < 0.001).

Conclusions:

The findings from this study suggest a potential effect of mistimed expressed breast milk consumption on an infant's circadian rhythm, affecting some aspects of their sleep. This is an important first step in exploring mistimed feeding on infant sleep outcomes and provides preliminary evidence that warrants future research.

Introduction

The benefits of breast milk have been shown to be highly protective of the mental and physical health of an infant.¹ In recent years, research has also shown that breast milk contains melatonin. Melatonin is a hormone that promotes sleep initiation and helps regulate the circadian rhythm by synchronizing our sleep–wake cycle between night and day.^2,3 Melatonin concentrations in breast milk clearly exhibit a 24-hour pattern that aligns with the mother's circadian timing.^4–6 Normal melatonin production in individuals starts around 9:00pm and peaks at around 2:00–3:00am in the morning, returning to minimal levels during the day. This is similar to the levels of melatonin found in breast milk, with daytime breast milk having minimal to nonexistent melatonin but high concentrations in the evening, peaking around 3:00am.^4,6,7

In addition, cortisol, which promotes alertness, is found in daytime breast milk.⁸ Unlike breast milk, infant milk formula provides no circadian timing, with product lines currently having no night blends that contain melatonin. Commonly, past research exploring sleep outcomes of infants who were breastfed versus formula fed reports that exclusive breastfeeding was associated with more night-time awakenings, sleep onset difficulties,⁹ and shorter sleep duration at night compared with formula-fed infants.^10,11 Past research, however, has not distinguished clearly between expressed breastfeeding and feeding directly from the breast, combining them together under one category,^12,13 therefore, has not considered the timing. Research that has considered partially breastfed infants (a combination of breast milk, formula and/or animal milk) showed that partially breastfed infants slept fewer hours and had more night awakenings, when compared with exclusively breastfed infants.¹⁴

Human circadian rhythm regulates a range of bodily functions, including an individual's sleep and feeding patterns, alertness, core body temperature, urine production, cell regeneration, and many other biological activities. For an infant, however, the circadian sleep–wake rhythm is not established, taking ∼3 months postbirth to fully develop.^4,15 The presence of a circadian rhythm in breast milk suggests that fluctuations in melatonin levels throughout the day and night might be providing circadian rhythm signals to calibrate the infant circadian biology.^4,16

With the advent of breast pumps and refrigeration, ∼30–70% of mothers now express breast milk.^17,18 This provides mothers with the possibility to provide their breast milk to their infants at a different time from when it was expressed, resulting in the infant receiving “mistimed” hormonal breast milk. For example, breast milk expressed in the morning might be fed to an infant at night and conversely, breast milk expressed at night might be fed to an infant during the day. If breast milk is providing circadian rhythm signals to infants, consuming mistimed breast milk may potentially desynchronize an infant's circadian timing, similar to that experienced by adults who engage in shift work or experience jet lag.^19,20

Although there is evidence that the hormonal composition of breast milk changes over the course of the day,^4,21 little is known about the impact of this on infants' health, particularly sleep, if consumed at the wrong time of day. Approximately 20–30% of parents report that their infant or child experiences sleep problems within their first few years of life, such as difficulty falling asleep at the start of the night, frequent night awakenings, early morning waking, or a combination of these.^9,22,23 Infants with poor sleep patterns (shorter sleep duration, difficulty with sleep onset, and more awakenings) are at an increased risk of obesity,²⁴ early onset or risk of type 2 diabetes later in life, poor mental health,^25,26 behavior problems, and autism spectrum disorders.^27,28 Therefore, the role and impact of mistimed expressed breast milk consumption on an infant's circadian rhythm development needs attention.

To our knowledge, no study has explored the impact that mistimed expressed breast milk consumption has on infant sleep outcomes. The aim of this study was to explore whether infant consumption of mistimed express breast milk has an impact on infant sleep outcomes. The preliminary nature of this research, in that it is the first known study to test the theory of circadian rhythm messaging to infants through breast milk, will inform the worth and nature of conducting future and larger research in this area. It was hypothesized that infants who consume mistimed expressed breast milk will experience poorer sleep outcomes (sleep quality, duration, sleep onset, and awakenings), compared with infants who consume other feeding types.

Materials and Methods

A cross-sectional study design was used, involving an anonymous online survey. The study was approved by the La Trobe University ethics committee on the May 11, 2021 (HEC21091). Data were collected between July and August 2021. Mothers who were 18 years and over, living in Australia, who had an infant that they were currently breastfeeding or formula feeding, were invited to participate in an online survey. The survey was promoted through social media (e.g., Facebook targeting parent support groups, mothers groups), was voluntary, anonymous, and took ∼20 minutes to complete. The participant information and consent form was embedded within the survey. Informed consent was obtained by asking participants to tick a box that they had read the form and consented to participation before beginning the survey.

In this study, the following data were collected: Mother and infant characteristics: Participants were asked questions about their and their infant's characteristics. Questions included asking the mother for their age (years), height, weight, location of residence (metropolitan or rural location), whether they had been diagnosed sleep disorder (yes/no) or postnatal depression diagnosis (yes/no), and for their infant's age (weeks) and delivery type (vaginal birth, elective or planned cesarean, or emergency cesarean).

Feeding type: The following general infant feeding questions, based on a mother's regular feeding type for the past 4 weeks, were asked: Which option below best fits how you regularly feed your infant? (a) Direct breastfed, which is feeding directly from the breast, (b) Combination of breastfed and expressed/pumped breast milk, (c) Expressed/pumped only, (d) Formula only, (e) Combination of breastfed and formula fed, (f) Combination of expressed and formula, (g) Combination of all, or (h) Other—Please specify.

Mistimed expressed breast milk: Mothers answering yes to any combination of the aforementioned question relating to expressed breast milk were also asked the following questions to determine whether consumption was timed or mistimed: What time of the day do you normally express/pump? and What time of the day does your infant normally get fed expressed/pumped breast milk? The response options to these questions were the same for both: (a) Normally in the morning (6:00am–12:00pm), (b) Normally in the afternoon (12:00–6:00pm), (c) Normally at night-time/early morning (7:00pm–1:00am), (d) Normally in the early morning (2:00–5:00am), (e) All of the above, (f) Randomly anytime, or (g) Other—please specify.

If the times were different or random between the two questions, then they were considered “mistimed.” The Brief Infant Sleep Questionnaire-Revised (The BISQ-R):^29,30 The BISQ-R was also used to assesses duration of sleep, night-time awakenings and whether the infant has a sleep problem, based on parental reporting, during the past 2 weeks. The BISQ-R has been validated against sleep diaries and objectively with actigraphy and designed to be administered to parents of children aged up to 3 years of age.²⁹

Statistical analysis

Statistical analyses were performed using statistical software for social sciences (SPSS) statistical package (version. 27) for Windows (SPSS, Inc., Chicago, IL). Research Electronic Data Capture (REDcaps), an online web application for building and managing online surveys was used to administer the survey. Raw data were exported from REDcaps into an excel document where it was transferred to SPSS for analysis. Summary statistics were performed, which included mean ± standard deviation (SD) and frequencies (n, %). Feeding types were coded into five groups: (1) direct breastfed only, (2) formula only, (3) express mistimed, (4) express-timed, and (5) breastfed/formula. Univariate analysis was undertaken on characteristics and sleep outcomes across the whole sample.

A one-way analysis of variance (ANOVA) and Bonferroni post hoc test was used on continuous variables to test differences in characteristics and sleep outcomes of continuous variables and the five feeding types. Chi square (χ²) tests were performed on categorical and ordinal variables of interest to assess differences between feeding types and sleep outcomes. Assumptions, such as normality, and outliers were checked. No outliers were observed. Where homogeneity of variance was not met, the Brown–Forsythe test was performed, and a backward regression was then undertaken to compare against any significant variables. A p-value <0.05 was considered statistically significant.

Results

A total of 329 mothers completed the survey. Mothers had a mean age of 32 years (SD ±5.7), mean body mass index of 26.7 (SD ±5.7) and the infants mean age was 24 weeks (SD ±3.2). The characteristics and clinical features of the participating mothers and their infants are outlined in Table 1.

Table 1.

Maternal and Infant Characteristics and Clinical Features (n = 329)

Variable	Mean ± SD/n (%)
Infant's age (weeks)	24.4 ± 3.2
Mother's age (years)	32 ± 5.7
Mother's BMI	26.7 ± 5.7
Mode of birth^*
Vaginal birth	220 (66.9)
Emergency cesarean	65 (19.8)
Elective/planned cesarean	44 (13.3)
Residential area^*
Metropolitan	239 (72.6)
Regional/rural	90 (27.1)
Diagnosed postnatal depression^*
No	300 (91.2)
Yes	29 (8.8)
Diagnosed sleep disorder at any time^*
No	327 (99.4)
Yes	2 (0.6)
Usual feeding type^*
Direct breastfed	169 (51.5)
Formula	20 (6.1)
Mistimed expressed breast milk	78 (23.8)
Timed expressed breast milk	32 (9.8)
Combination breastfed/formula	29 (8.8)
Do you think your infant has a sleep problem?^*
A very serious problem	7 (2.1)
A small problem	100 (30.4)
Not a problem at all	189 (57.4)

Continuous variables were summarized by mean (SD), categorical variables were summarized by frequency and % represented by ^*n (%).

BMI, body mass index; SD, standard deviation.

Results from the ANOVA (Table 2), comparing the five feeding types showed a significant difference between feeding types in sleep onset, that is, the minutes it took for the infant to get to sleep at night (p < 0.001) and in the average night-time awakenings (p < 0.001). Bonferroni post hoc tests for multiple comparisons showed that infants who consumed mistimed expressed breast milk took significantly longer to get to sleep compared with infants who were directly breastfed (p < 0.001), formula fed (p = 0.002), fed timed expressed breast milk (p < 0.001), and fed breast milk/formula combined (p = 0.023). Breastfed infants had significantly more awakenings at night compared with infants who consumed formula (p < 0.001) and mistimed expressed breast milk (p < 0.001).

Table 2.

Outcome of One-Way Analysis of Variance Comparing Infant Feeding Types with Group Characteristics and Sleep–Wake Variables (Mean ± Standard Deviation)

	Feeding type
	Direct breastfed	Formula	Mistimed expressed breast milk	Timed expressed breast milk	Combination breast/formula	F	p
Age of infant	24.98 ± 15.86	26.65 ± 12.20	20.41 ± 13.35	27.75 ± 17	24.72 ± 15.87	1.93	0.11
Age of mother	32.02 ± 2.99	33.10 ± 4.14	31.65 ± 3.29	32.06 ± 2.21	33.34 ± 3.98	1.61	0.17
BMI	26.14 ± 5.59	26.68 ± 5.71	27.49 ± 5.06	26.93 ± 5.92	27.19 ± 6.46	0.828	0.51
Location^*
Metro	123 (74)	10 (50)	48 (62.3)	31 (96.9)	24 (82.8)	20.43	<0.001
Regional/rural	44 (26)	10 (50)	29 (37.7)	1 (3.1)	5 (17.2)	20.43	<0.001
Have you been diagnosed with postnatal depression?^*
Yes	15 (8.9)	1 (5)	7 (9)	2 (6.3)	3 (10.3)	0.70	0.95
No	154 (91.1)	19 (95)	71 (91)	30 (93.8)	26 (89.7)	0.70	0.95
Started solid food^*
Yes	86 (53.1)	13 (65)	28 (35.9)	16 (50)	19 (65.5)	10.80	0.029
No	83 (49.1)	7 (35)	50 (64.1)	16 (50)	10 (34.5)	10.80	0.029
Have you been diagnosed with a sleep disorder?^*
Yes	1 (0.5)	1 (5)	0 (0)	0 (0)	0 (0)	7.21	0.13
No	168 (99.4)	19 (95)	78 (100)	32 (100)	29 (100)	7.21	0.13
Average minutes to get to sleep at night	18.87 ± 10.7	15.53 ± 8.9	31.01 ± 22.9	15.78 ± 10.4	19.52 ± 12.2	9.67	<0.001
Average number of night awakenings	2.84 ± 1.5	1.29 ± 1.0	1.93 ± 1.3	2.6 ± 1.7	2.0 ± 0.9	8.97	<0.001
Average total night sleep duration (minutes)	535.73 ± 206.7	554.25 ± 246.5	543.65 ± 200.1	589.69 ± 177.8	567.14 ± 202.1	0.569	0.69
Average total night awake duration (minutes)	49.43 ± 45.8	51.75 ± 87.4	44.17 ± 41.9	47.03 ± 51.2	43.62 ± 43.3	0.243	0.91
Average total day sleep duration (minutes)	193.21 ± 117.8	182.25 ± 128.6	233.46 ± 150.3	200.47 ± 97.1	223.48 ± 122.6	2.08	0.08
Do you think your infant has a sleep problem?^*
Not a problem	92 (60.5)	12 (70.6)	47 (68.1)	18 (60)	19 (70.4)	5.71	0.69
A small problem	57 (37.5)	5 (29.4)	20 (29)	10 (33.3)	8 (29.6)
A serious problem	3 (2)	0 (0)	2 (2.9)	2 (6.7)	0 (0)

One-way analysis of variance where appropriate, otherwise chi square analysis indicated by ^*n (%). Significance in bold at p < 0.05.

BMI, body mass index.

The χ² analysis found that there was a significant difference between the five feeding types depending on location (metropolitan/rural) (p = 0.001), with a higher percentage of mistimed expressed breast milk for infants living in rural areas, compared with metropolitan infants. There was also a significant difference between feeding types and whether the infants had started solid foods (p = 0.03), with 35.9% of infants in the mistimed expressed breast milk group having started solid foods compared with 50–65.5% from the other groups (Table 2). A backward regression model, controlling for age and those infants on solid food, found that the total daytime sleep duration (minutes; p = 0.03) of the infant, sleep onset at night (minutes; p = 0.04) and average awakenings per night (p < 0.001) remained significant [F(3,260) = 7.10, p < 0.001]. The model explained 7.6% (Nagelkerke R² 0.076) of the variance between feeding types.

Discussion

The findings from this study support our hypothesis that consuming mistimed expressed breast milk may affect certain infant sleep outcomes. Infants who consumed mistimed expressed breast milk took significantly longer (12.5 minutes) to get to sleep at night (sleep onset), compared with infants who consumed other feeding types. Longer sleep onset time for infants who consumed mistimed breast milk aligns to the known function of melatonin, which is promoting sleep initiation.^2,3 In addition, infants who consumed mistimed breast milk at night might also be consuming daytime breast milk, which is high in cortisol, a hormone that promotes alertness.⁸

Although not statistically significant (p = 0.08), infants in our study who were given mistimed expressed breast milk also slept ∼40 minutes longer during the daytime than those infants who directly breastfed, which is still clinically noteworthy. This helps support our theory that the hormonal content of breast milk may assist with the development of an infant's circadian rhythm, thus infants who receive mixed signals could have their sleep affected. Direct breastfed infants, however, had significantly more night-time awakenings than formula-fed infants, which is consistent with other research.^9–11

The importance of these findings could be substantial, not just during the first few months of an infant's circadian development, but in later months too. Melatonin has been widely used as a biomarker for circadian desynchronization.³¹ If an infant consumes mistimed expressed breast milk regularly, there may be a risk of disrupting their natural sleep–wake cycle over time. This may result in similar effects experienced by adult who work shift work or have a circadian rhythm misalignment sleep disorder (CRMSD) such as delayed sleep phase disorder.^32,33 Adults with a CRMSD often experience excessive daytime sleepiness, fatigue, irritability, or impaired cognitive function,^34,35 and are at greater risk of health issues such as obesity, type 2 diabetes, and depression.^31,36,37

Past research has shown that infant's age and starting solid food may have an influence on sleep outcomes such as sleeping longer at night and having less awakenings.^38,39 The results from this study found no significant differences in infant's age between the five feeding types, but there was a significant difference in whether they had started solid food. Although past research suggests that infants who have started solid food are more likely to sleep longer, awake less at night, and have shorter sleep onset times than those who have not started solid food,³⁸ this study found feeding type (mistimed breast milk), and not solid food, was the main influence of sleep onset. This suggests that delayed sleep onset might be related more to the concept of mistimed expressed breast milk and lack of melatonin, rather than whether infants had started solid food.

Results from this study, however, need to be interpreted with caution by considering the following limitations. This study was a cross-sectional study, with a reliance on subjective, self-reported responses, and so no causal relationship can be drawn. It is recommended that to improve reliability, future research should objectively measure the circadian timing of the infant and mother, such as through saliva samples and actigraphy as well as measure the level of melatonin in breast milk. Furthermore, prospectively logging the time mothers express and when they give expressed breast milk would more accurately measure mistimed milk consumption.

The results are an important first step in exploring the proposed theory that the hormones in breast milk may serve as an indicator of day/night to infants and lends to the development of their circadian rhythm and supports the hypothesis that mistimed expressed breast milk feeding could impact on sleep outcomes. The study provides preliminary evidence that future research is needed in this area.

It is recommended that the next step is to undertake a large-scale research project objectively measuring melatonin and cortisol levels in expressed breast milk at different times and measuring the transfer of these hormones to the infant. In addition, exploration as to the long-term potential consequences to the infant if consuming mistimed expressed breast milk is warranted. This research could help inform best practice guidelines and policy regarding the handling, storage, and provisioning regarding the circadian changes in breast milk composition over the day. Labeling the time of expression of the breast milk could reduce any potential timing problems; however, currently there are no relevant guidelines for mothers and no procedures and policies in place at Donor Banks to take into consideration the timing of breast milk expression. Furthermore, infant milk formula currently has no day and night blend, but infants and parents may benefit if both types became available on the market.

Conclusion

This study showed that there is a potential effect of mistimed expressed breast milk consumption on an infant's sleep onset, which is worth further investigation. It is hoped that outcomes from this study will generate awareness and highlight issues of mistimed expressed breast milk feeding, directing future research opportunities, and inform best practice recommendations around timing and labeling of expressed breast milk.

Footnotes

Acknowledgments

The team would like to thank all the mothers who took time out to complete the survey.

Authors' Contributions

L.B., J.S., M.D.C., and T.S. were responsible for study design, data interpretation, and composing and editing the article. L.B. and M.D.C. performed the analysis and J.S. and T.S. contributed to the interpretation. All authors were involved in preparing the article. All authors approved the final article as submitted and agree to be accountable for all aspects of the study.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

World Health Organization. Infant and Young Child Feeding. 2020, 2021. Available from: https://www.who.int/news-room/fact-sheets/detail/infantand-young-child-feeding (accessed May 28, 2022).

Pevet

, Challet

Melatonin: Both master clock output and internal time-giver in the circadian clocks network. J Physiol, 2011; 105(4–6):170–182; doi: 10.1016/j.jphysparis.2011.07.001

Pandi-Perumal

, Srinivasan

, Spence

, et al. Role of the melatonin system in the control of sleep. CNS Drugs, 2007; 21(12):995–1018; doi: 10.2165/00023210-200721120-00004

Illnerová

, Buresová

, Presl

Melatonin rhythm in human milk. J Clin Endocrinol Metab, 1993; 77(3):838–841; doi: 10.1210/jcem.77.3.8370707

Katzer

, Pauli

, Mueller

, et al. Melatonin concentrations and antioxidative capacity of human breast milk according to gestational age and the time of day. J Hum Lact, 2016; 32(4):NP105–NP110; doi: 10.1177/0890334415625217

Cubero

, Valero

, Sánchez

, et al. The circadian rhythm of tryptophan in breast milk affects the rhythms of 6-sulfatoxymelatonin and sleep in newborn. Neuro Endocrinol Lett, 2005; 26(6):657–661. PMID: 16380706.

Engler

, Hadash

, Shehadeh

, et al. Breastfeeding may improve nocturnal sleep and reduce infantile colic: Potential role of breast milk melatonin. Eur J Pediatr, 2011; 171(4):729–732; doi: 10.1007/s00431-011-1659-3

Pundir

, Wall

, Mitchell

, et al. Variation of human milk glucocorticoids over 24hour period. J Mammary Gland Biol Neoplasia, 2017; 22(1):85–92; doi: 10.1007/s10911-017-9375-x

Messayke

, Davisse-Paturet

, Nicklaus

, et al. Infant feeding practices and sleep at 1year of age in the nationwide ELFE cohort. Matern Child Nutr, 2021; 17(1):e13072; doi: h10.1111/mcn.13072

10.

Figueiredo

, Dias

, Pinto

, et al. Exclusive breastfeeding at three months and infant sleep-wake behaviors at two weeks, three and six months. Infant Behav Dev, 2017;49:62–69; doi: 10.1016/j.infbeh.2017.06.006

11.

Rudzik

AEF

, Robinson-Smith

, Ball

. Discrepancies in maternal reports of infant sleep vs. actigraphy by mode of feeding. Sleep Med, 2018; 49:90–98; doi: 10.1016/j.sleep.2018.06.010

12.

AIHW. 2010. Australian National Infant Feeding Survey: Indicator Results. In: Australian Institute of Health and Welfare. (ed.) AIHW: Canberra, Australia; 2011; p. 4.

13.

WHO. Indicators for Assessing Infant and Young Child Feeding Practices. In: Organization WH. (ed.) World Health Organization: Washington DC, USA; 2008; pp. 3–5.

14.

Huang

, Wang

, Chang

, et al. Feeding methods, sleep arrangement, and infant sleep patterns: A Chinese population-based study. World J Pediatr, 2016; 12(1):66–75; doi: 10.1007/s12519-015-0012-8

15.

Mirmiran

, Maas

, Ariagno

. Development of fetal and neonatal sleep and circadian rhythms. Sleep Med Rev, 2003; 7(4):321–334; doi: 10.1053/smrv.2002.0243

16.

Anderson

, Vaillancourt

, Maes

, et al. Breast feeding and melatonin: Implications for improving perinatal health. J Breastfeed Biol, 2016; 1(1):8–20; doi: 10.14302/issn.2644-0105.jbfb-16-1121

17.

Labiner-Wolfe

, Fein

, Shealy

, et al. Prevalence of breast milk expression and associated factors. Pediatrics, 2008;122 Suppl 2:S63–S68; doi: 10.1542/peds.2008-1315h

18.

Johns

, Amir

, McLachlan

, et al. Breast pump use amongst mothers of healthy term infants in Melbourne, Australia: A prospective cohort study. Midwifery, 2016;33:82–89; doi: 10.1016/j.midw.2015.10.009

19.

Zee

, Goldstein

. Treatment of shift work disorder and jet lag. Curr Treat Options Neurol, 2010; 12(5):396–411; doi: 10.1007/s11940-010-0090-9

20.

Drake

, Wright

. Shift

Work

, Shift-Work

Disorder

, and Jet

Lag

. In: Principles and Practice of Sleep Medicine (5th Edition), Elsevier

Saunders

, St. Louis: 2011; pp. 784–798.

21.

Italianer

, Naninck

EFG

, Roelants

, et al. Circadian variation in human milk composition: A systematic review. Nutrients, 2020; 12(8):2328; doi: 10.3390/nu120823288

22.

Sette

, Baumgartner

, Ferri

, et al. Predictors of sleep disturbances in the first year of life: A longitudinal study. Sleep Med, 2017;36:78–85; doi: 10.1016/j.sleep.2017.04.015

23.

Byars

, Yolton

, Rausch

, et al. Prevalence, patterns, and persistence of sleep problems in the first 3 years of life. Pediatrics, 2012; 129(2):e276–e284; doi: 10.1542/peds.2011-0372

24.

Petrovic

, Spatharakis

, Conroy

, et al. Prevalence of sedative drug use in geriatric in-patients: A multi-centre study. Acta Clin Belg, 2006; 61(3):119–126; doi: 10.1179/acb.2006.019

25.

Mah

, Larkings

Association between poor sleep for infants to two years and subsequent mental health symptoms: A systematic review and meta-analysis. J Child Health Care, 2021; 26(3):461–478; doi: 10.1177/13674935211015085

26.

Marino

, Andrade

, Campisi

, et al. Association between disturbed sleep and depression in children and youths: A systematic review and meta-analysis of cohort studies. JAMA Netw Open, 2021; 4(3):e212373–e212373; doi: 10.1001/jamanetworkopen.2021.2373

27.

Reynolds

, Soke

, Sabourin

, et al. Sleep problems in 2- to 5-year-olds with autism spectrum disorder and other developmental delays. Pediatrics, 2019; 143(3):e20180492; doi: 10.1542/peds.2018-0492

28.

Carmassi

, Palagini

, Caruso

, et al. Systematic review of sleep disturbances and circadian sleep desynchronization in autism spectrum disorder: Toward an integrative model of a self-reinforcing loop. Front Psychiatry (Systematic Review), 2019;10:366; doi: 10.3389/fpsyt.2019.00366

29.

Sadeh

A brief screening questionnaire for infant sleep problems: Validation and findings for an internet sample. Pediatrics, 2004; 113(6):e570–e577; doi: 10.1542/peds.113.6.e570

30.

Mindell

, Gould

, Tikotzy

, et al. Norm-referenced scoring system for the Brief Infant Sleep Questionnaire—Revised (BISQ-R). Sleep Med, 2019;63:106–114; doi: 10.1016/j.sleep.2019.05.010

31.

Mirick

, Davis

. Melatonin as a biomarker of circadian dysregulation. Cancer Epidemiol Biomarkers Prev: A publication of the American Association for Cancer

Research

, cosponsored by the American Society of Preventive

Oncology

. 2008; 17(12):3306–3313; doi: 10.1158/1055-9965.epi-08-0605

32.

American Academy of Sleep Medicine. International Classification of Sleep Disorders: Diagnostic and Coding Manual (3rd Edition) (ICSD-3). American Academy of Sleep Medicine: Darien, IL, USA; 2014.

33.

Bjorvatn

, Pallesen

A practical approach to circadian rhythm sleep disorders. Sleep Med Rev, 2009; 13(1):47–60; doi: 10.1016/j.smrv.2008.04.009

34.

Boivin

, Boudreau

Impacts of shift work on sleep and circadian rhythms. Pathol Biol, 2014; 62(5):292–301; doi: 10.1016/j.patbio.2014.08.001

35.

Drake

, Roehrs

, Richardson

, et al. Shift work sleep disorder: Prevalence and consequences beyond that of symptomatic day workers. Sleep, 2004; 27(8):1453–1462; doi: 10.1093/sleep/27.8.1453

36.

Antunes

, Jornada

, Ramalho

, et al. Correlation of shift work and waist circumference, body mass index, chronotype and depressive symptoms. Arq Bras Endocrinol Metabol, 2010; 54(7):652–656; doi: 10.1590/s0004-27302010000700010

37.

Mason

, Qian

, Adler

, et al. Impact of circadian disruption on glucose metabolism: Implications for type 2 diabetes. Diabetologia, 2020; 63(3):462–472; doi: 10.1007/s00125-019-05059-6

38.

Perkin

, Bahnson

, Logan

, et al. Association of early introduction of solids with infant sleep: A secondary analysis of a randomized clinical trial. JAMA Pediatr, 2018; 172(8):e180739–e180739; doi: 10.1001/jamapediatrics.2018.0739

39.

Bruni

, Baumgartner

, Sette

, et al. Longitudinal study of sleep behavior in normal infants during the first year of life. J Clin Sleep Med, 2014; 10(10):1119–1127; doi: 10.5664/jcsm.4114