Links between infant sleep and parental tolerance for infant crying: longitudinal assessment from pregnancy through six months postpartum

Accepted Manuscript Links between infant sleep and parental tolerance for infant crying: longitudinal assessment from pregnancy through 6months postpartum Michal Kahn, Yasmin Bauminger, Ella Volkovich, Gal Meiri, Avi Sadeh, Liat Tikotzky PII:

S1389-9457(18)30201-6

DOI:

10.1016/j.sleep.2018.05.014

Reference:

SLEEP 3705

To appear in:

Sleep Medicine

Received Date: 20 February 2018 Revised Date:

11 May 2018

Accepted Date: 14 May 2018

Please cite this article as: Kahn M, Bauminger Y, Volkovich E, Meiri G, Sadeh A, Tikotzky L, Links between infant sleep and parental tolerance for infant crying: longitudinal assessment from pregnancy through 6months postpartum, Sleep Medicine (2018), doi: 10.1016/j.sleep.2018.05.014. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Links between infant sleep and parental tolerance for infant crying: longitudinal assessment from pregnancy through 6 months postpartum

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Michal Kahn a, Yasmin Bauminger b, Ella Volkovich b, Gal Meiri c, Avi Sadeh a, Liat Tikotzky b ,*

The School of Psychological Sciences, Tel Aviv University, Tel Aviv, Israel

b

Department of Psychology, Ben-Gurion University of the Negev, Beer-Sheva, Israel

c

Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel

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a

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* Corresponding author. Department of Psychology Ben-Gurion University of the Negev, Beer-Sheva, Israel +972-54-5497243 E-mail address: [email protected] (L. Tikotzky).

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Avi Sadeh, one of the main contributors to this study, passed away in September of 2016.

ABSTRACT

Background: Low parental tolerance for crying has been associated with infant sleep problems, yet the directionality of this link remained unclear. This longitudinal study aimed to assess the synchronous and prospective bidirectional links between parental cry-tolerance, soothing, and infant sleep from pregnancy through 6 months postpartum. 1

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Methods: Sixty-five couples were recruited during pregnancy and assessed for cry-tolerance using a paradigm in which participants are shown a videotape of a crying infant and are asked to stop the video when they feel it is necessary to intervene. Infant sleep was assessed objectively

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using actigraphy for five nights at 3 and 6 months postpartum. Parental soothing techniques were reported by parents at both assessment points, and cry-tolerance was reassessed at 6 months. Results: Concomitant associations were found between maternal cry-tolerance and infant sleep at

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6 months, indicating that lower maternal cry-tolerance was correlated with poorer actigraphic sleep quality. Furthermore, Structural Equation Modeling analyses yielded significant

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prospective associations, showing that lower cry-tolerance at pregnancy predicted better infant sleep at 3 months, whereas more disrupted sleep at 3 months predicted lower cry-tolerance at 6 months. Additionally, fathers showed higher cry-tolerance compared to mothers, and parents became more similar to each other across time in their reactivity to infant crying.

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Conclusion: Consistent with the transactional model of infant sleep, the findings of this study highlight the role of parental cry-tolerance in infant sleep development, and demonstrate

Keywords:

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Infant sleep

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bidirectional links between this construct and infant sleep throughout the first 6 months of life.

Infant crying Actigraphy Parents

Parental sensitivity Longitudinal study

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1. Introduction

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Young infants are often thought of as powerless, helpless beings, yet they are actually equipped with one of the most powerful tools in human repertoire – their ability to cry. Crying is a

universal form of early communication, which promotes parental proximity and enhances

chances of survival [1,2]. Neuroimaging studies have documented strong activation in “parental-

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brain networks” in response to infant crying, including areas underlying reward and motivational

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processes, empathic responding, and emotional regulation [3–6]. Infant crying has also been shown to elicit physiological arousal in adults, manifested in cardiac acceleration, increased skin conductance, and endocrine changes [7,8]. Parents’ cognitive and behavioral responses to crying may be affected by various factors, including parenting experience [9], parental psychopathology [10,11], and parent gender [12,13]. For instance, women are more likely to intervene in response

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to infant crying compared to men [13].

The ways in which parents respond to infant crying may have a substantial impact on the parent–child relationship and on child development in various domains [14–16]. Specifically,

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infant behavioral sleep-related problems (eg, recurrent night-wakings) are highly associated with both infant crying and parenting practices [17], yet there is a dearth of studies exploring the link

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between parental reactivity to crying and infant sleep. It is well documented that parents play a key role in the development of infant sleep

[18,19]. Infants of parents who are more actively involved in settling their infant to sleep have been shown to present more behavioral sleep-related problems compared to infants with parents who are less active at bedtime [19,20]. Burnham and colleagues [21] found that longer parental response times to infant night-wakings at 3 months predicted better self-soothing abilities at

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12 months of age. In another longitudinal study of the first year of life, mothers who tended to interpret infant night-wakings at 6 months as a sign of distress that requires immediate attention were more likely to actively soothe their infants to sleep at 12 months, and these infants were

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more likely to experience night-wakings [20]. These findings suggest that parental difficulty in withholding their response to infant awakenings (commonly manifested in crying) may hinder the development of infant self-soothing abilities that promote better sleep [20,22,23].

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Accordingly, interventions for infant sleep problems usually target parental cognitions and

behaviors at bedtime in an attempt to reduce parental involvement and promote the development

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of infant self-soothing. The effectiveness of such interventions has been extensively established, and they often involve the parent’s ability to tolerate some extent of crying at night [24–26]. In an initial attempt to directly examine the association between parental cry-tolerance (PCT) and infant sleep problems, Sadeh and coworkers [27] found that parents of infants with

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clinically fragmented sleep were less tolerant to infant crying (ie, intervened faster to stop a film of a crying infant when they believed that the infant should be soothed) compared to parents of infants without sleep problems, and to childless controls. In addition, women in this study

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demonstrated lower tolerance for infant crying compared to men. These findings suggest that PCT may be an important factor in the development of infant sleep. However, due to the

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correlative nature of this study, it does not allow for conclusions regarding directionality. For example, it is plausible that the links between PCT and infant sleep are bidirectional. Bidirectional links between parenting behaviors, parental cognitions, and infant sleep have been demonstrated before and are in line with the transactional model of infant sleep development [20,28,29]. Accordingly, on the one hand, low parental tolerance for crying may predict greater infant dependence on parental soothing and thus higher levels of expressed sleep-related

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problems. On the other hand, infant sleep problems that entail excessive crying may influence parents’ responsiveness and tolerance for crying. The present study aims to broaden the understanding of these associations by examining the transactional links between maternal and

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paternal PCT and objective infant sleep from pregnancy through 6 months postpartum.

Specifically, the goals of this longitudinal study were to examine (1) changes in infant sleep from 3 to 6 months; (2) changes in maternal and paternal PCT from pregnancy (representing pre-

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parenting PCT, still unaffected by the crying of their own infant) to 6 months; and (3)

prospective links between infant sleep, maternal soothing practices and PCT using objective

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measures of sleep.

We hypothesized that actigraphy-based infant sleep would become more consolidated from 3 to 6 months. In accordance with the recent findings of Sadeh and colleagues [27], we additionally predicted that both parents’ PCT would decrease with time, and that mothers would

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present lower PCT compared to fathers. Finally, we expected to find concomitant and

infant sleep.

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2. Methods

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bidirectional predictive associations between lower PCT and more disturbed actigraphy-based

2.1. Participants

Sixty-five expectant couples were recruited for this study during the third trimester (weeks 34– 37) of their first pregnancy. Participants were recruited through hospital prenatal courses and through advertisements in internet forums for expectant parents. The sample included only twoparent families with singleton pregnancy. Table 1 presents the sample characteristics. The 5

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socioeconomic characteristics (ie, education level of parents, and number of rooms in the house) suggest that the sample was mostly representative of middle-upper socioeconomic status in Israel. None of the participant demographic characteristics were consistently associated with

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PCT, maternal soothing, or infant sleep, and thus they were not controlled for in subsequent statistical analyses.

Mean ± SD

Range

Mother’s age (years)

28.20±3.16

21–35

Mother’s education (years)

15.84±1.76

12–19

Father’s age (years)

29.73±3.21

22–39

Father’s education (years)

15.33±2.40

12–22

Number of rooms in the

3.37±0.95

2–6

house

(weeks)

Child sex

3.22±0.42

2.20–4.71 52.3% (N=34) girls

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2.2. Procedures

34.5–42

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Child birth weight (kg)

39.44±1.35

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Child gestational age

%

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Demographic

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Table 1. Sample characteristics

The study was approved by the hospital’s Helsinki Committee. Signed informed consent was obtained from all parents before participation. Home visits were held with each participating family at three assessment points: (1) third trimester of pregnancy; (2) 3 months postpartum; and (3) 6 months postpartum. Demographic characteristics were collected during the pregnancy assessment. PCT was assessed for each parent using the Intervention Delay to Infant Crying

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Video (IDICV) at pregnancy and at 6 months postpartum. Infant sleep was measured when infants were 3 and 6 months old using actigraphy. During the home visits, parents were given an actigraph and were instructed to attach it to their child’s ankle for five nights, and to keep a sleep

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diary during this period. Parents were asked to record sleep only on weekdays when a regular family routine was maintained. At the 3- and 6-month assessment points, mothers additionally completed the Parental Interactive Bedtime Behavior Scale (PIBBS), aimed at assessing the

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soothing behaviors they used when putting their child to sleep. After each assessment point

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parents received a small gift (value of $20), and a graphic report of their infant’s sleep.

2.3. Measures 2.3.1. Infant Sleep

Sleep was assessed using actigraphy, which has been established as a non-intrusive reliable

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method for naturalistic studies of sleep–wake patterns in infants, children, and adults [30,31]. The actigraph is a miniature wristwatch-like device that is attached to the infant’s ankle during the sleep period, and enables continuous recording of movements, which are later translated to

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valid sleep–wake measures. Participating parents were provided with actigraphs for their

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infants (Mini Motionlogger, Ambulatory Monitoring, Inc., Ardsley, NY, USA), with amplifier setting 18 and 1-min epoch interval according to the standard working mode for sleep–wake scoring. Sleep data were collected for five nights at the 3- and 6-month assessments. Data were analyzed using the Sadeh algorithm, which is the most commonly reported analysis method for infant populations [30,32]. Daily sleep diaries were completed during the assessment period, and were used to corroborate the actigraphic data, and to detect and correct any potential artifacts of these data. The following sleep parameters were used for this study: (1) sleep minutes: number 7

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of minutes during the sleep period that are scored as sleep; (2) nocturnal wakefulness: minutes spent in wakefulness between sleep onset and morning rise time; and (3) number of long waking episodes: night-wakings lasting a minimum of 5 min. All measures were averaged across the

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monitoring period.

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2.3.2. PCT

The IDICV [27] was used to assess PCT. In this procedure, participants are presented with a 2-

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min video clip of a crying infant, with gradually increasing crying intensity. Prior to watching the video, a written cover story is presented to the participants: “The following video is of a very demanding baby. His parents are trying to ignore some of his crying to allow him to calm himself down. Please look at the video and decide when you feel it is absolutely necessary to intervene.” The cover story was meant to create a standardized description of the situation, and

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to increase parental motivation to tolerate the crying and delay their response. We alternately used two versions of the IDICV; one in which the infant is positioned on a mattress during daytime, and one in which the infant is positioned in its crib during night-time. While watching the

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video, parents wore a headset, adjusted to an average of 80 db. The delay to intervene (in

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seconds) was used as the outcome measure for this procedure. Shorter delays represent lower PCT. Both parents completed this procedure independently at pregnancy and at the 6-month assessment.

2.3.3. Maternal Soothing Patterns

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A soothing questionnaire based on the PIBBS [33] was administered to mothers at 3 and 6 months postpartum to assess the strategies they use to settle their infants to sleep. The PIBBS includes 17 items on which parents rate soothing techniques on a five-point Likert-scale. In this

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study we combined two of the five subscales developed by Morrell and Cortina-Borja [33]; “active physical comforting” and “social comforting,” to create a general “active nighttime soothing” scale. This scale included eight items, such as “cuddling or rocking,” “patting

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child,” and “settling in parents’ bed.” This scale showed good internal consistency at each time

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point in the present study (at 3 months α = 0.78; at 6 months α = 0.80).

2.4. Statistical Analyses

Paired-samples t-tests were used to compare infant sleep at 3 and 6 months postpartum. Repeated measures analysis of variance (ANOVA) was used to examine changes in maternal and paternal

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cry-tolerance over time. Finally, Structural Equation Modeling (SEM) was used to test the predictive and concomitant links between infant sleep, maternal and paternal cry-tolerance and maternal soothing techniques at night-time within unified multidimensional models. SEM

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analyses were conducted using the Amos program (Version 7, Amos Development Corporation,

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Florida), using the maximum likelihood estimation method. All other analyses were performed using SPSS version 22.0 (IBM Corporation, USA). Out of the 65 participating families, six mothers (9.23%) and eight fathers (12.31%)

failed to complete the IDICV at 6 months, and valid actigraphic data were obtained from 58 infants at the 3-month assessment and 55 infants at the 6-month assessment. Missing data resulted from technical failures or inability of participants to complete the procedures within the predetermined infant’s age window. Using Little’s test [34] missing values were found to be 9

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missing completely at random (χ2(170) = 164.74, p=0.59). To preserve representativeness and size of the original sample and allow for statistical analysis of the same sample at both time points, multiple imputations were applied to complete missing data. The imputations were

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completed using the Markov chain Monte Carlo method [35].

3. Results

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3.1. Developmental changes in infant sleep from 3 to 6 months

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To assess the development of infant sleep, paired t-tests were conducted comparing actigraphic measures at 3 and 6 months of age. The results of these analyses are presented in Table 2. A significant difference was found in total minutes of sleep per night, indicating an increase in nocturnal sleep minutes from 3 to 6 months. In addition, the results indicate a significant decrease in minutes of nocturnal wakefulness from 3 to 6 months postpartum. No significant

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difference in the number of night-wakings was found from 3 to 6 months. Table 2. Means, standard errors, t- and p-values of the actigraphic sleep measures. 3 Months

Mean

Standar

6 Months Mean

d error

t (1, 59)

p

Standar d error

553.71

8.94

583.05

5.56

-3.35

0.001

Nocturnal wakefulness (in min)

48.99

2.69

42.57

3.55

2.01

0.04

Night-wakings (number)

2.78

0.16

2.53

0.22

1.20

0.23

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Sleep minutes

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Actigraphic sleep measures

3.2. Differences in maternal and paternal tolerance for infant crying between pregnancy and 6 months postpartum 10

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To assess differences between maternal and paternal PCT (intervention delays to the infant crying video) from pregnancy to 6 months, repeated measures ANOVA was conducted with time and parent as the independent variables, and PCT as the dependent variable (N=65). The main

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effect for time was significant, F(1, 64)=5.63, p=0.02, indicating that parental tolerance

significantly decreased from pregnancy to 6 months. The main effect for parent gender was also significant, F(1, 64)=4.97, p=0.03, indicating that fathers had significantly higher PCT than

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mothers. The parent gender by time interaction effect was insignificant F(1, 64)=3.06, p=0.08.

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(see Fig. 1).

Cry-tolerance (IDICV) 60 50 40

20 10 0

6 Months Postpartum

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Pregnancy

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30

Mothers

Fathers

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Fig.1. Means and standard error bars for maternal and paternal cry-tolerance meaured in seconds, using the Intervention Delay to Infant Crying Video (IDICV) at pregnany and 6 months postpartum.

3.3. Associations between PCT, maternal soothing behaviors, and infant sleep

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To examine the links between PCT, maternal soothing, and infant sleep we first calculated Pearson correlations between these variables (see Table 3).

1

Sleep minutes (3 months)

2.

Sleep minutes (6 months) Nocturnal wakefulness (3 months) Nocturnal wakefulness (6 months) Night-wakings (3 months)

3.

4.

5.

3

4

5

6

7

— 0.40 *

—

0.17

-0.10

—

0.12

0.22

0.47 **

—

0.31 *

0.06

0.89 **

0.49 **

—

8

9

10

11

12

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1.

2

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Measure

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Table 3. Correlations between maternal and paternal cry-tolerance at pregnancy and 6 months, infant sleep variables and maternal night-time soothing at 3 and 6 months.

Night-wakings (6 months)

0.01

0.18

0.43 **

0.87 **

0.42 *

—

7.

PCT – mothers pregnancy

0.12

0.04

0.25

0.00

0.26 *

0.02

—

8.

PCT – mothers (6 months)

0.02

0.10

-0.40 *

-0.26 *

-0.29 *

-0.33 *

0.07

—

9.

PCT – fathers pregnancy

0.09

-0.10

0.02

-0.21

-0.06

-0.15

0.14

0.28 *

—

10. PCT – fathers (6 months)

0.07

0.21

-0.25

-0.13

-0.13

-0.16

-0.08

0.55 **

0.45 **

—

11. Active soothing (3 months)

-0.09

0.06

0.07

0.07

0.15

0.08

0.13

0.01

-0.10

-0.01

12. Active soothing (6 months)

0.02

0.13

0.12

0.22

0.18

0.22

0.05

-0.26 *

-0.05

0.03

0.63 **

—

SD

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Mean

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6.

N (imputed values)

—

553.71

583.05

48.99

42.57

2.78

2.53

37.68

34.13

51.00

36.89

3.28

2.92

66.81

40.13

20.39

26.04

1.23

1.58

31.99

27.59

40.14

26.68

0.98

0.97

65 (7)

65 (10)

65 (7)

65 (10)

65 (7)

65 (10)

65 (0)

65 (6)

65 (0)

65 (8)

65 (5)

65 (8)

PCT, parental cry-tolerance; SD, standard deviation. *p <0.05, **p <0.005.

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Overall, the correlations reflect concomitant and predictive associations between maternal cry-tolerance and the two objective measures of sleep quality, namely nocturnal wakefulness and the number of waking episodes, indicating that lower maternal cry-tolerance

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was associated with poorer infant sleep quality. Sleep quantity, as measured by the number of minutes during the sleep period, was not significantly correlated with PCT, and thus was not included in subsequent analyses of these associations.

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Next, we conducted SEM analyses to assess the predictive multivariate relationships between infant sleep, maternal and paternal cry-tolerance, and maternal soothing techniques at

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night-time. Because of the limited sample size (N=65), we chose to use only observed variables and focused on each of the two objective measures of sleep quality. We included synchronous (cross-sectional), stability (autoregressive) and most importantly longitudinal paths in each of the SEM models [36].

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Good fit indices were obtained for the SEM models presented in Fig. 2. For Model A, depicting the links between PCT, maternal soothing techniques, and infant nocturnal wakefulness: χ2(8)  was  9.75, p=0.28, normed fit index (NFI) was 0.91, comparative fit index

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(CFI) was 0.97, and root mean square error of approximation (RMSEA) was 0.06. For Model B, depicting the links between PCT, maternal soothing techniques and infant night-waking

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episodes: χ2(8)  was  6.88, p=0.55, NFI was 0.93, comparative fit index CFI was 1.00, and RMSEA was 0.00.

Both models demonstrate significant links between PCT, infant sleep, and maternal

soothing at night. In Model A, infant wakefulness at night and maternal soothing behaviors remained stable from 3 to 6 months (β=0.47, p<0.001; β=0.62, p<0.001, respectively). Paternal cry-tolerance was stable over time (β=0.33, p=0.002); however, maternal cry-tolerance was not

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(β=0.18, not significant). Maternal cry-tolerance at pregnancy was significantly correlated with infant nocturnal wakefulness at 3 months (β=0.26, p=0.04), whereas paternal cry-tolerance was not (β=-0.03, not significant). Interestingly, the direction of this link was positive, indicating that

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infants of mothers that were more sensitive (less tolerant) to crying at pregnancy tended to be less wakeful during the night at 3 months. Nocturnal wakefulness at 3 months predicted both maternal and paternal cry-tolerance at 6 months (β=-0.42, p<0.001; β=-0.25, p=0.04,

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respectively). As hypothesized, these correlations were negative, indicating that parents of infants that spent more time awake at 3 months were less tolerant to crying at 6-months.

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Longitudinal effects between PCT and maternal soothing were non-significant, but a synchronous effect was found at 6 months between soothing behavior and maternal cry-tolerance (β=-0.35, p=0.01) indicating that higher active soothing was associated with lower maternal crytolerance. Finally, while maternal and paternal cry-tolerance were not significantly correlated at

p=0.002).

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pregnancy, a significant correlation between these variables was found at 6 months (β=0.47,

Model B, predicting the number of night-wakings, yielded similar results. Significant

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stability effects were found for paternal cry-tolerance, number of night-wakings, and maternal

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soothing (β=0.32, p=0.002; β=0.42, p<0.001; β=0.63, p<0.001, respectively). As with nocturnal wakefulness, greater maternal but not paternal cry sensitivity (lower tolerance) at pregnancy predicted less infant night-wakings at 3 months postpartum (β=0.29, p=0.02). In addition, more infant night-wakings at 3 months significantly predicted lower maternal cry-tolerance at 6 months (β=-0.31, p=0.01), but the equivalent link was not significant for fathers’ cry-tolerance (β=-0.13, not significant). Finally, synchronous effects were found at 6 months between soothing

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behavior and maternal cry-tolerance (β=-0.34, p=0.02), as well as between maternal and paternal

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cry-tolerance (β=0.51, p<0.001).

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Fig. 2. Structural Equation Models illustrating associations between parental cry-tolerance (PCT), maternal soothing techniques and infant nocturnal wakefulness (Model A), and number of night waking episodes (Model B). Standardized coefficients are presented in the figures. *p<0.05, **p<0.005.

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4. Discussion This is, to the best of our knowledge, the first study focusing on the longitudinal links between

measured infant sleep from pregnancy to 6 months postpartum.

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parental (both maternal and paternal) cry-tolerance, maternal soothing practices, and objectively

Our findings demonstrate the anticipated consolidation in infant sleep from 3 to 6 months of

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age, manifested in a significant increase in nocturnal sleep minutes and decrease in nocturnal wakefulness. These changes reflect maturation processes that have been documented in previous

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investigations of sleep in the early postpartum months [37,38].

As expected, PCT significantly decreased over time, as demonstrated in the shorter delays in intervening with the videotaped crying infant at 6 months compared to pregnancy. This finding dovetails well with Sadeh and colleagues’ [27] results that showed reduced PCT in parents of normally developing infants compared to childless married couples. The finding is also

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consistent with the developmental pattern of parental cognitions found in Tikotzky and Sadeh’s longitudinal study [20], indicating that during pregnancy mothers place more emphasis on the

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importance of limiting parental night-time involvement to encourage infant self-soothing, than they do at 6 months. Thus, it seems that after becoming a parent and accumulating experiences

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with a baby of their own, parents become more sensitive to infant signs of distress. In line with our hypothesis regarding parent gender, fathers exhibited higher PCT compared to mothers. This finding is consistent with previous investigations demonstrating higher tolerance to infant crying and distress in men compared to women [13,27,39]. Furthermore, our results yielded a significant correlation between maternal and paternal PCT at 6 months, whereas the equivalent correlation at pregnancy was insignificant. This suggests that mothers and fathers become more similar to each other over time in their reactivity to infant crying. This growing 17

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similarity may be a result of shared experiences with their own child, including mutual discussions and reciprocal modeling of responses to their crying infant. Earlier studies have

results broaden this literature to the domain of PCT.

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documented enhances in childrearing similarity between parents across time [40,41], and our

Overall and consistent with Sadeh et al. [27], our results support the hypotheses regarding the links between PCT, infant sleep, and maternal soothing, particularly regarding PCT in mothers.

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When measured concurrently at 6 months, maternal PCT and infant sleep were significantly correlated. Specifically, infants of mothers who presented longer delays in intervening with the

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filmed crying infant had significantly fewer night-wakings and shorter nocturnal wakefulness. Maternal PCT was also negatively correlated with soothing techniques, such that greater cryingtolerance was associated with less actively involved maternal soothing of the infant to sleep. Regarding the predictive links between sleep and PCT, SEM analyses revealed significant

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bidirectional longitudinal links from pregnancy through 3 and 6 months. Interestingly, lower PCT at pregnancy predicted better sleep at 3 months, whereas more disrupted sleep at 3 months predicted lower PCT at 6 months. This shift in directionality may be explained by the evolving

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needs of the infant throughout the first months of life, and the emerging capacity to self-regulate. Higher PCT during late pregnancy may induce premature parental expectations for infant self-

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soothing to sleep, that may lead to less attuned parenting and to poorer sleep at 3 months. This idea is consistent with findings demonstrating that parental responsiveness in the early months promotes early infant self-regulation, including sleep regulation. For instance, early maternal responsiveness at bedtime has been found to predict better infant physiological regulation at 3 months [42]. In accordance with these notions, most behavioral interventions for infant sleeprelated problems do not recommend starting in the early postpartum months, due to the

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heightened dependency of infants on the parent for regulation, their feeding needs, and the rapid maturation of sleep during this period [25,26,43]. These ideas also allude to van IJzendoorn and Hubbard’s [44] concept of “differential responsiveness”, stressing the importance of context

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(e.g., the infant’s developmental level or the intensity of crying) in determining which parental response is most appropriate. Moreover, in their investigation of the associations between crying and maternal responsiveness, these authors concluded that these links are bidirectional. That is,

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not only do parents affect their infants, but infants also influence and shape their parents

behaviors. Complex and reciprocal interactions between parental and infant behavior in the

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context of infant sleep development have been demonstrated before [19]. For example, in a recent study, Philbrook and Teti found that lower levels of nursing at bedtime predicted an increase in infant night-time sleep during the first 6 months [28]. However, there was also evidence for infant-driven effects as infant night-time distress was a significant predictor of

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maternal emotional availability. Accordingly, our results revealed that more disturbed infant sleep at 3 months predicts lower PCT at 6 months of age. Thus, parents may become more sensitive to infant crying when they have to continuously take care of a night-waking infant.

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This study has several limitations that merit consideration. First, the design did not include an assessment of PCT at 3 months. Thus, cross-lagged associations between PCT at 3 months and

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sleep at 6 months could not be examined. Second, the IDICV was used as the sole measure of PCT. Future investigations could use various measures of PCT to capture different aspects (eg, cognitive, physiological) of parental reactivity to crying. Finally, the sample was relatively small and homogeneous, thus limiting statistical power and restricting the generalizability of the results.

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Conclusions Taken together, our findings provide support for the construct of PCT and its role in objective infant sleep development, and demonstrate for the first time bidirectional prospective links

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between PCT and sleep. These findings could inform early intervention, as they underscore the importance of the timing chosen for treatment. Increasing PCT may have different effects on infant sleep if targeted early or later in the infant’s first year of life. Specifically, our findings

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suggest that increasing PCT may lead to better infant sleep if targeted after the age of 3 months, but not before that. More work is needed to test these postulations, to further examine the

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development of PCT and its associations with infant sleep across longer periods of time, and to

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explore the mechanisms that underlie these bidirectional associations.

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Conflict of interest

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The authors have no conflicts of interest to disclose.

Acknowledgements

This study was supported by a grant from the Israel Science Foundation (Grant number

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1075/10). We wish to thank all participating families and all the students who helped with data

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collection.

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References [1] Bell SM, Ainsworth MDS. Infant crying and maternal responsiveness. Child Dev. 1972:1171-90. [2] Bowlby J. Attachment and Loss: Attachment: Hogarth, London; 1969.

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[3] Feldman R. The adaptive human parental brain: implications for children's social development. Trends Neurosci. 2015;38:387-99.

[4] Swain JE. The human parental brain: in vivo neuroimaging. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35:1242-54.

[5] Seifritz E, Esposito F, Neuhoff JG, Lüthi A, Mustovic H, Dammann G, et al. Differential sex-

SC

independent amygdala response to infant crying and laughing in parents versus nonparents. Biol Psychiatry. 2003;54:1367-75.

[6] Firk C, Dahmen B, Lehmann C, Herpertz-Dahlmann B, Konrad K. Down-regulation of Amygdala

M AN U

Response to Infant Crying: A Role for Distraction in Maternal Emotion Regulation. Emotion (Washington, DC). 2017.

[7] Del Vecchio T, Walter A, O’Leary SG. Affective and physiological factors predicting maternal response to infant crying. Infant Behav Dev. 2009;32:117-22.

[8] Groh AM, Roisman GI. Adults’ autonomic and subjective emotional responses to infant vocalizations: The role of secure base script knowledge. Dev Psychol. 2009;45:889.

TE D

[9] Stallings J, Fleming AS, Corter C, Worthman C, Steiner M. The effects of infant cries and odors on sympathy, cortisol, and autonomic responses in new mothers and nonpostpartum women. Parenting. 2001;1:71-100.

[10] Riem MM, Pieper S, Out D, Bakermans-Kranenburg MJ, van IJzendoorn MH. Oxytocin receptor

EP

gene and depressive symptoms associated with physiological reactivity to infant crying. Soc Cogn Affect Neurosci. 2010;6:294-300.

[11] Schuetze P, Zeskind PS. Relations between women's depressive symptoms and perceptions of infant

AC C

distress signals varying in pitch. Infancy. 2001;2:483-99. [12] Frodi AM, Lamb ME, Leavitt LA, Donovan WL, Neff C, Sherry D. Fathers' and mothers' responses to the faces and cries of normal and premature infants. Dev Psychol. 1978;14:490. [13] Boukydis CZ, Burgess RL. Adult physiological response to infant cries: Effects of temperament of infant, parental status, and gender. Child Dev. 1982:1291-8. [14] Wolff MS, van Ijzendoorn MH. Sensitivity and attachment: A meta‐analysis on parental antecedents of infant attachment. Child Dev. 1997;68:571-91. [15] Leerkes EM, Parade SH, Gudmundson JA. Mothers' emotional reactions to crying pose risk for subsequent attachment insecurity. J Fam Psychol. 2011;25:635.

22

ACCEPTED MANUSCRIPT

[16] Williams CJ, Kessler D, Fernyhough C, Lewis G, Pearson RM. The association between maternalreported responses to infant crying at 4 weeks and 6 months and offspring depression at 18: a longitudinal study. Arch Womens Ment Health. 2016;19:401-8. [17] Smart J, Hiscock H. Early infant crying and sleeping problems: A pilot study of impact on parental

RI PT

well‐being and parent‐endorsed strategies for management. J Paediatr Child Health. 2007;43:284-90. [18] Touchette É, Petit D, Tremblay RE, Montplaisir JY. Risk factors and consequences of early childhood dyssomnias: New perspectives. Sleep Med Rev. 2009;13:355-61.

[19] Sadeh A, Tikotzky L, Scher A. Parenting and infant sleep. Sleep Med Rev. 2010;14:89-96.

pregnancy through the 1st Year. Child Dev. 2009;80:860-74.

SC

[20] Tikotzky L, Sadeh A. Maternal sleep‐related cognitions and infant sleep: A longitudinal study from

[21] Burnham MM, Goodlin‐Jones BL, Gaylor EE, Anders TF. Nighttime sleep‐wake patterns and self‐

M AN U

soothing from birth to one year of age: A longitudinal intervention study. J Child Psychol Psychiatry. 2002;43:713-25.

[22] Sadeh A, Flint-Ofir E, Tirosh T, Tikotzky L. Infant sleep and parental sleep-related cognitions. J Fam Psychol. 2007;21:74.

[23] Morrell JM. The role of maternal cognitions in infant sleep problems as assessed by a new instrument, the maternal cognitions about infant sleep questionnaire. J Child Psychol Psychiatry. 1999;40:247-58.

TE D

[24] Hiscock H, Wake M. Randomised controlled trial of behavioural infant sleep intervention to improve infant sleep and maternal mood. BMJ. 2002;324:1062. [25] Mindell JA, Kuhn B, Lewin DS, Meltzer LJ, Sadeh A. Behavioral treatment of bedtime problems and night wakings in infants and young children. Sleep. 2006;29:1263-76.

EP

[26] Gradisar M, Jackson K, Spurrier NJ, Gibson J, Whitham J, Williams AS, et al. Behavioral interventions for infant sleep problems: A randomized controlled trial. Pediatrics. 2016:e20151486.

AC C

[27] Sadeh A, Juda‐Hanael M, Livne‐Karp E, Kahn M, Tikotzky L, Anders TF, et al. Low parental tolerance for infant crying: an underlying factor in infant sleep problems? J Sleep Res. 2016;25:501-7. [28] Philbrook LE, Teti DM. Bidirectional associations between bedtime parenting and infant sleep: Parenting quality, parenting practices, and their interaction. J Fam Psychol. 2016;30:431. [29] Sadeh A, Anders TF. Infant sleep problems: Origins, assessment, interventions. Infant Ment Health J. 1993;14:17-34.

[30] Sadeh A. The role and validity of actigraphy in sleep medicine: an update. Sleep Med Rev. 2011;15:259-67. [31] Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollak CP. The role of actigraphy in the study of sleep and circadian rhythms. Sleep. 2003;26:342-92.

23

ACCEPTED MANUSCRIPT

[32] Meltzer LJ, Montgomery-Downs HE, Insana SP, Walsh CM. Use of actigraphy for assessment in pediatric sleep research. Sleep Med Rev. 2012;16:463-75. [33] Morrell J, Cortina‐Borja M. The developmental change in strategies parents employ to settle young children to sleep, and their relationship to infant sleeping problems, as assessed by a new questionnaire:

RI PT

The Parental Interactive Bedtime Behaviour Scale. Infant Child Dev. 2002;11:17-41. [34] Little RJ. A test of missing completely at random for multivariate data with missing values. J Am Stat Assoc. 1988;83:1198-202.

[35] Schafer JL, Graham JW. Missing data: our view of the state of the art. Psychol Methods. 2002;7:147.

wave, cross-lagged study. J Consult Clin Psychol. 2003;71:890.

SC

[36] Shahar G, Davidson L. Depressive symptoms erode self-esteem in severe mental illness: a three-

[37] Henderson JM, France KG, Blampied NM. The consolidation of infants' nocturnal sleep across the

M AN U

first year of life. Sleep Med Rev. 2011;15:211-20.

[38] Galland BC, Taylor BJ, Elder DE, Herbison P. Normal sleep patterns in infants and children: a systematic review of observational studies. Sleep Med Rev. 2012;16:213-22. [39] Young KS, Parsons CE, LeBeau RT, Tabak BA, Sewart AR, Stein A, et al. Sensing emotion in voices: Negativity bias and gender differences in a validation study of the Oxford Vocal (‘OxVoc’) sounds database. Psychol Assess. 2017;29:967.

[40] Holden GW, Miller PC. Enduring and different: a meta-analysis of the similarity in parents' child

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rearing. Psychol Bull. 1999;125:223.

[41] Horvath CA, Lee CM, Bax K. How similar are mothers and fathers of young children in their parenting responses and goals? J Child Fam Stud. 2015;24:3542-51. [42] Philbrook LE, Hozella AC, Kim B-R, Jian N, Shimizu M, Teti DM. Maternal emotional availability

EP

at bedtime and infant cortisol at 1 and 3 months. Early Hum Dev. 2014;90:595-605. [43] Tikotzky L, Sadeh A. The role of cognitive–behavioral therapy in behavioral childhood insomnia. Sleep Med. 2010;11:686-91.

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[44] van IJzendoorn MH, Hubbard FO. Are infant crying and maternal responsiveness during the first year related to infant-mother attachment at 15 months? Attach Hum Dev. 2000;2:371-91.

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Links between infant sleep and parental tolerance for infant crying:

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Longitudinal assessment from pregnancy through 6 months postpartum

Highlights

The links between parental cry-tolerance and infant sleep are bidirectional.

Lower maternal cry-tolerance at pregnancy predicted better infant sleep at 3 months.

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Poorer infant sleep at 3 months predicted lower cry-tolerance at 6 months.

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Fathers demonstrated higher cry-tolerance compared to mothers.

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• • • •