Understanding the concurrent and predictive relations between child-led emotion regulation behaviors and pain during vaccination in toddlerhood : PAIN

Journal Logo

Research Paper

Understanding the concurrent and predictive relations between child-led emotion regulation behaviors and pain during vaccination in toddlerhood

Gennis, Hannah G.a; Flora, David B.a; Norton, Lucasa; McMurtry, C. Meghanb,c,d,e; Merlano, Tatiana Espinosaa; Zaghi, Ameera; Flanders, Danielf; Weinberg, Eitanf; Savlov, Deenaf; Garfield, Hartleyf,g; Pillai Riddell, Rebecca R.a,f,g,*

Author Information
PAIN 164(6):p 1291-1302, June 2023. | DOI: 10.1097/j.pain.0000000000002816

1. Introduction

Pediatric pain researchers have long been interested in understanding and reducing children's pain.1,32,37,46 Given the importance of parents during painful procedures19,31 and the developing attachment relationship5 in infancy and toddlerhood, work in these developmental periods has typically focused on how parental factors (eg, soothing behaviors, sensitivity) reduce children's pain-related distress,2–4,11,23,27,28,33,34 with less focus on child behaviors that may regulate distress.4 Parental sensitivity and soothing does not fully explain children's distress after a painful procedure, with research showing small to moderate effects on acute pain-related distress in infancy and early toddlerhood.28,33

To understand emotion regulation, researchers must observe an emotion, behaviors that modify the emotion, and how these relate over time.13,16,45 In early infancy, strategies to reduce distress are largely caregiver-led; however, as they transition to toddlerhood, children begin a shift from caregiver-led emotion regulation to more active involvement in their own emotion regulation.25,26,40,41 Child-led emotion regulation behaviors have been coded in experimental contexts,10,39,43 allowing researchers to understand which child behaviors reduce distress across development. As shown in a recent literature review,20 there is evidence that in infancy, physical self-soothing behaviors (eg, thumb sucking) reduce distress.7,18,43 As children develop into toddlerhood, disengagement of attention (eg, orienting to or manipulating a non–task-related object) is more strongly associated with reductions in distress compared with infancy,6,8,14,22 whereas positive associations with parent-focused behaviors (eg, orienting to parent) suggest that toddlers may signal a need for support to their parent.6,9,15

Vaccination, a routine painful procedure, allows repeated opportunities to understand the development of child-led emotion regulation in a naturalistic context and may also help researchers expand their understanding of factors that reduce children's pain. Consistent with past research in preschool children,12 the goal of the current article is to assess both the concurrent and the predictive relations between child-led emotion regulation behaviors and pain-related distress immediately after routine vaccination across the second year of life at both 12 and 18 months. Toddlers and their parents were video-recorded during their vaccination visit, and videos were subsequently coded for child-led emotion regulation behaviors and pain-related distress.

The following research question was targeted:

  • (1) How do children's disengagement of attention, parent-focused strategies, and physical self-soothing strategies relate to pain-related distress concurrently (ie, within the same timepoint) and predictively (from 1 timepoint to the next) at 1, 2, and 3 minutes postneedle?

We hypothesized that disengagement of attention and physical self-soothing strategies would show negative relations with pain-related distress after vaccination, whereas parent-focused behaviors would show a positive relationship. Differences in associations at 12 and 18 months were also explored.

2. Methods

2.1. Participants

Data collection for the current analyses occurred between September 2015 and March 2020, as part of a longitudinal cohort study.47 Caregiver–toddler dyads were recruited from 2 pediatric clinics in the Greater Toronto Area. The study followed a cohort-sequential design during which dyads were observed at their 12-, 18-, and 24-month vaccination appointments. The current study includes data from the 12- and 18-month vaccinations. Ethics approval was obtained through the research ethics board at the participating university. Caregivers were approached by a research assistant who explained the study and went over informed consent. Toddlers were recruited before their 12- or 18-month vaccination appointments and were followed up at subsequent appointments. Figure 1 outlines recruitment and loss of participants. To be included in the current analyses, codable video data were required for each dyad, resulting in a total of 163 caregiver–toddler dyads at 12 months and 149 caregiver–toddler dyads at 18 months. Table 1 outlines key demographic variables, which demonstrates that the sample predominantly included mothers from well-educated, middle-class families. The cultural diversity of the sample is generalizable to the broader Greater Toronto Area population.42

F1
Figure 1.:
Participant flow chart.
Table 1 - Demographic information by age.
12 mo 18 mo
Child sex
 Male 85 (52.8) 86 (58.5)
 Female 76 (47.2) 61 (41.5)
Relationship to child
 Mother 146 (90.7) 127 (85.8)
 Father 14 (8.7) 20 (13.5)
 Other 1 (0.6) 1 (0.7)
Caregiver education
 Graduate school or professional training 82 (52.9) 70 (54.3)
 University graduate (4 y) 47 (30.3) 38 (29.5)
 Partial university (at least 1 y) 3 (1.9) 3 (2.3)
 Trade school/community college 20 (12.9) 17 (13.2)
 High school graduate 3 (1.9) 1 (0.8)
Parents' age (y) 35.21 (5.09); 20-59 36.27 (5.97); 22-62
Heritage culture
 Asian 38 (25.2) 34 (23.3)
 European 37 (24.5) 37 (25.3)
 North American 32 (21.2) 33 (22.6)
 Latin, Central, and South American 7 (4.6) 4 (2.7)
 Oceanian 3 (2.0) 2 (1.4)
 Caribbean 2 (1.3) 1 (0.7)
 African 1 (0.7) 3 (2.1)
 Mixed 20 (13.2) 21 (14.4)
 Other ethnic and cultural origin 11 (7.3) 11 (7.5)
Acculturation
 Lifestyle reflects mainstream Canadian culture 7.7 (2.19); 0-10 7.8 (1.94); 1-10
 Lifestyle reflects heritage culture 6.65 (2.70); 0-10 5.82 (2.49); 0-10
Child sex, relationship to child, caregiver education, and heritage culture are presented as frequency (percentage). Parent age and acculturation status are presented as mean (SD); range.

2.2. Procedure

The current study includes only behavioral data. However, at each appointment, dyads were videotaped and connected to equipment to measure their cardiac response. Toddlers and caregivers were recorded for at least 3 minutes postneedle. Given the naturalistic observation methodology, there was minimal interference from the research team during vaccination appointments, other than the video and physiological recording. Research assistants did not interact with participants during the vaccination window. At each vaccination appointment, caregivers were given an information sheet outlining evidence-based pain management strategies for toddlers.44

2.3. Measures

2.3.1. Demographic information

Before the vaccination, caregivers completed a demographic questionnaire that asked for child's age, child's sex, caregiver's age, relationship to the child, and caregiver's education. Caregivers also identified their heritage culture and then were asked, how much they identified with that heritage culture (on a scale from 0 to 10) and how much they identified with mainstream Canadian culture (also on a scale from 0 to 10).

2.3.2. Toddler emotion regulation behaviors

Emotion regulation behaviors were coded from video footage using the coding system from the Laboratory Temperament Assessment Battery (Lab-TAB) Locomotor Version 3.1.21 The Lab-TAB is a well-established and valid10,17,35,39 developmental psychology protocol designed to capture a comprehensive repertoire of childhood emotion-related measures through a series of experimental procedures meant to invoke a variety of different emotions in infants and toddlers (eg, fear). The authors worked with the current Lab-TAB coordinator and trainer (Dr. Jeffrey Gagne, Texas A&M University) to adapt the child-led emotion regulation behaviors subset to fit the vaccination context. A subset of 6 behaviors was ultimately included. These behaviors were object orientation, proximity-seeking, caregiver orientation, thumb sucking, other oral behavior, and physical touch. See Table 2 for a description of each behavior and examples. Each behavior was coded as present (1) or absent (0) in 5-second epochs for the 1-minute period after the last needle, 2-minute period after the last needle, and 3-minute period after the last needle.

Table 2 - Description of emotion regulation behaviors.
Emotion regulation behavior Description
Object orientation Child independently orients away from the procedure (eg, swabbing, needle, vaccinating health professional) and orients to or manipulates a nonprocedure-related object in the environment (eg, orients to or manipulates a caregiver's cellphone or points to the door)
Caregiver orientation Child directly looks towards a caregiver (eg, hears his or her caregiver's voice and turns his or her head towards caregiver)
Proximity-seeking Child initiates an attempt to get closer to caregiver (eg, leaning head towards caregiver's chest, verbally saying “Mama,” and reaching arms towards mother)
Thumb sucking Child puts a part of own body (eg, thumb, finger, fist) in mouth and either sucks or moves it around inside
Other oral behavior Child uses an object in his or her mouth (eg, pacifier, bottle) without a caregiver actively feeding it to him or her
Touch body Child actively touches or rubs a part of own body (eg, rubbing arm, rubbing belly, rubbing face, wiping eyes) for the purpose of soothing

Scores were calculated representing the proportion of intervals a given behavior was present out of the total number of codable epochs within each 1-minute time period. These scores ranged from 0 to 1, with higher scores indicating higher frequency of that behavior. Coding was completed using Noldus Observer, a behavioral coding computer program. Twenty percent of the 12- and 18-month combined sample was double-coded to assess interrater reliability. Percentage (and kappa) agreement ranged as follows for each behavior: object orientation = 0.83 to 0.85 (κ = 0.58-0.63), proximity-seeking = 0.87 to 0.93 (κ = 0.71-0.81), caregiver orientation = 0.88 to 0.91 (κ = 0.63-0.74), thumb sucking = 0.98 to 0.99 (κ = 0.74-0.91), other oral behavior = 0.98 to 0.99 (κ = 0.94-0.96), and physical touch = 0.92 to 0.95 (κ = 0.66-0.82). Coders were blind to study hypotheses. Based on a review of the experimental literature,20 the current analyses combined the 6 Lab-TAB behaviors into 3 clusters of self-regulatory behaviors: disengagement of attention (object orientation), parent-focused behaviors (proximity-seeking and caregiver orientation), and physical self-soothing (thumb sucking, other oral behaviors, and physical touch) for 1, 2, and 3 minutes postneedle.

2.3.3. Pain-related distress

The Face, Legs, Activity, Cry, Consolability (FLACC29) coding system was used to measure the degree of behavioral pain-related distress postimmunization. The FLACC was used to assess 5 types of pain behaviors in 15-second increments consecutively over the 3-minute period of post-needle observation. Within each epoch, each of the 5 behaviors was scored on a 0 to 2 scale, resulting in a total score from 0 to 10 for each 15 seconds. To get a score for each post-needle minute, the four 15-second epochs within that minute were averaged. Coding was also completed using the Noldus Observer. Research has demonstrated moderate to high concurrent validity and interrater reliability for FLACC scores in the acute pain context.29,30 Twenty percent of the current sample was double-coded throughout the coding process to assess interrater reliability between coders at 12 and 18 months, which was strong (intraclass correlation coefficient [ICC]= 0.93-0.96). Coders were blind to study hypotheses.

2.4. Analysis plan

To examine the concurrent and predictive relations among the 3 clusters of emotion regulation behaviors and pain-related distress at both 12 and 18 months, 6 separate autoregressive cross-lagged path models24 (3 emotion regulation behaviors [disengagement of attention, parent-focused behaviors, and physical self-soothing] by 2 ages [12 and 18 months]) were estimated using the lavaan package38 in R.36 These models were specified so that 3 types of relations were estimated simultaneously: (1) Predictive Within-Measure, (2) Predictive Between-Measure, and (3) Concurrent (Residual) Between-Measure. First, autoregressive Predictive Within-Measure relations assess the prediction of the behavior (either emotion regulation or pain-related distress behavior) from the measure of the same behavior that directly preceded it (eg, Disengagement of Attention Minute 1 predicting Disengagement of Attention Minute 2). Second, the cross-lagged Predictive Between-Measure relations assess the prediction of an emotion regulation behavior from the pain-related distress behavior that directly preceded it (or prediction of the pain-related distress behavior from the directly preceding emotion regulation behavior; eg, FLACC Minute 1 predicting Disengagement of Attention Minute 2, and Disengagement of Attention Minute 1 Predicting FLACC Minute 2). Finally, Concurrent (Residual) Between-Measure relations assess the simultaneous relations between the emotion regulation behavior and pain-related distress behavior at each of the 3 minutes, controlling the autoregressive and cross-lagged effects (eg, concurrent relationship between FLACC Minute 1 and Disengagement of Attention Minute 1). The models were estimated using full-information maximum likelihood to allow the inclusion of incomplete cases and robust model fit statistics, and SEs were used to account for nonnormality.38 The comparative fit index (CFI), the Tucker–Lewis index (TLI), and the root mean square error of approximation (RMSEA) were used to assess model fit.

3. Results

3.1. Descriptive statistics

Mean values and SDs of all variables in the 12- and 18-month models are presented in Table 3. Tables 4 and 5 present correlations among the variables included in each 12- and 18-month model, separated by emotion regulation cluster.

Table 3 - Descriptive statistics at 12 and 18 months.
12 mo 18 mo
N Mean (SD) Min Max N Mean (SD) Min Max
Disengagement of Attention 1 163 0.62 (0.24) 0 1 149 0.66 (0.25) 0 1
Disengagement of Attention 2 163 0.78 (0.26) 0 1 149 0.78 (0.26) 0 1
Disengagement of Attention 3 163 0.82 (0.25) 0 1 149 0.81 (0.27) 0 1
Parent Focused 1 163 0.33 (0.19) 0 0.83 149 0.25 (0.20) 0 0.79
Parent Focused 2 163 0.26 (0.23) 0 1 149 0.24 (0.20) 0 0.79
Parent Focused 3 163 0.24 (0.23) 0 1 149 0.25 (0.23) 0 1
Physical self-soothe 1 163 0.08 (0.10) 0 0.36 149 0.12 (0.12) 0 0.47
Physical self-soothe 2 163 0.12 (0.13) 0 0.56 149 0.12 (0.13) 0 0.5
Physical self-soothe 3 163 0.13 (0.14) 0 0.64 149 0.14 (0.15) 0 0.61
FLACC 1 162 6.69 (1.92) 0.5 10 149 5.48 (2.41) 0 9.19
FLACC 2 162 4.49 (2.66) 0 9 149 3.56 (2.79) 0 8.75
FLACC 3 161 2.97 (2.67) 0 8.75 149 2.83 (2.78) 0 9.75
For all variables, 1, 2, and 3 indicate 1, 2, and 3 minutes postneedle, respectively. FLACC represents pain-related distress.
FLACC, Face, Legs, Activity, Cry, Consolability.

Table 4 - Correlations among emotion regulation behaviors and pain-related distress at 12 months.
1 2 3 4 5 6 7 8 9 10 11 12
1. Disengagement of Attention 1
2. Disengagement of Attention 2 0.36*
3. Disengagement of Attention 3 0.18 0.49*
4. Parent-Focused 1 −0.19 −0.25 −0.12
5. Parent-Focused 2 −0.08 −0.29* −0.32* 0.54*
6. Parent Focused 3 −0.09 −0.32* −0.49* 0.47* 0.68*
7. Physical Self-Soothing 1 0.03 0.05 0.09 −0.07 0.13 0.03
8. Physical Self-Soothing 2 0.12 −0.04 −0.04 0.06 0.22 0.21 0.63*
9. Physical Self-Soothing 3 0.05 −0.06 −0.14 0.02 0.12 0.14 0.34* 0.60*
10. FLACC 1 −0.15 −0.05 −0.03 0.16 0.10 0.10 −0.27* −0.28* −0.06
11. FLACC 2 −0.14 −0.10 −0.09 0.25 0.22 0.18 −0.19 −0.23 −0.05 0.70*
12. FLACC 3 −0.04 −0.08 −0.12 0.21 0.15 0.23 −0.16* −0.14 −0.14 0.46* 0.66*
Because of concerns with type 1 error inflation, correlations with higher P values are not indicated.
*P < 0.001.
FLACC, Face, Legs, Activity, Cry, Consolability.

Table 5 - Correlations among emotion regulation behaviors and pain-related distress at 18 months.
1 2 3 4 5 6 7 8 9 10 11 12
1. Disengagement of Attention 1
2. Disengagement of Attention 2 0.40*
3. Disengagement of Attention 3 0.31* 0.60*
4. Parent-Focused 1 −0.18 −0.12 −0.22
5. Parent-Focused 2 −0.17 −0.24 −0.24 0.65*
6. Parent Focused 3 −0.15 −0.12 −0.32* 0.53* 0.62*
7. Physical Self-Soothing 1 0.06 0.14 0.14 −0.15 −0.07 −0.11
8. Physical Self-Soothing 2 0.06 0.09 0.15 −0.10 −0.08 −0.08 0.73*
9. Physical Self-Soothing 3 0.05 0.12 0.09 −0.03 −0.07 −0.11 0.64* 0.76*
10. FLACC 1 −0.17 −0.29* −0.14 0.38* 0.31* 0.24 −0.20 −0.15 −0.12
11. FLACC 2 −0.09 −0.14 −0.06 0.26 0.30* 0.18 −0.24 −0.18 −0.20 0.64*
12. FLACC 3 −0.07 −0.19 −0.11 0.20 0.26 0.21 −0.10 −0.09 −0.13 0.45* 0.76*
Because of concerns with type 1 error inflation, correlations with higher P values are not indicated.
*P < 0.001.
FLACC, Face, Legs, Activity, Cry, Consolability.

3.2. Models examining pain-related distress with child-led emotion regulation behaviors

Figures 2–7 present path diagrams, along with standardized estimates, for the 6 different models estimated. Tables 6–11 present the standardized and unstandardized estimates for these models. Each model fit the corresponding data adequately; see Table 12 for the fit statistics of each model.

F2
Figure 2.:
Model of disengagement of attention and pain-related distress at 12 months. Solid paths are significant with P < 0.05. Nonsignificant paths are dashed. FLACC, Face, Legs, Activity, Cry, Consolability.
F3
Figure 3.:
Model of disengagement of attention and pain-related distress at 18 months. Solid paths are significant with P < 0.05. Nonsignificant paths are dashed. FLACC, Face, Legs, Activity, Cry, Consolability.
F4
Figure 4.:
Model of parent-focused behaviors and pain-related distress at 12 months. Solid paths are significant with P < 0.05. Nonsignificant paths are dashed. FLACC, Face, Legs, Activity, Cry, Consolability.
F5
Figure 5.:
Model of parent-focused behaviors and pain-related distress at 18 months. Solid paths are significant with P < 0.05. Nonsignificant paths are dashed. FLACC, Face, Legs, Activity, Cry, Consolability.
F6
Figure 6.:
Model of physical self-soothing and pain-related distress at 12 months. Solid paths are significant with P < 0.05. Nonsignificant paths are dashed. FLACC, Face, Legs, Activity, Cry, Consolability.
F7
Figure 7.:
Model of physical self-soothing and pain-related distress at 18 months. Solid paths are significant with P < 0.05. Nonsignificant paths are dashed. FLACC, Face, Legs, Activity, Cry, Consolability.
Table 6 - Estimates for model of disengagement of attention and pain-related distress behavior at 12 months.
Standardized estimate Unstandardized estimate Z value P
Predictors FLACC 2 outcome
 FLACC 1 0.69 0.96 13.89 0.00
 D of A 1 −0.04 −0.45 −0.77 0.44
Disengagement of Attention 2 outcome
 D of A 1 0.36 0.39 4.25 0.00
 FLACC 1 0.01 0.00 0.10 0.92
FLACC 3 outcome
 FLACC 2 0.66 0.66 12.01 0.00
 D of A 2 −0.02 −0.17 −0.31 0.76
Disengagement of Attention 3 outcome
 D of A 2 0.49 0.48 4.66 0.00
 FLACC 2 −0.04 −0.00 −0.53 0.60
FLACC is the measure of pain-related distress.
D of A, Disengagement of Attention; FLACC, Face, Legs, Activity, Cry, Consolability.

Table 7 - Estimates for model of relationship between disengagement of attention and pain-related distress behavior at 18 months.
Standardized estimate Unstandardized estimate Z value P
Predictors FLACC 2 outcome
 FLACC 1 0.64 0.74 11.48 0.00
 D of A 1 0.03 0.28 0.39 0.70
Disengagement of Attention 2 outcome
 D of A 1 0.36 0.39 4.70 0.00
 FLACC 1 −0.23 −0.03 −3.42 0.00
FLACC 3 outcome
 FLACC 2 0.74 0.74 14.26 0.00
 D of A 2 −0.09 −0.93 −1.32 0.19
Disengagement of Attention 3 outcome
 D of A 2 0.60 0.62 8.30 0.00
 FLACC 2 0.03 0.00 0.39 0.70
FLACC is the measure of pain-related distress.
D of A, Disengagement of Attention; FLACC, Face, Legs, Activity, Cry, Consolability.

Table 8 - Estimates for model of relationship between parent-focused behaviors and pain-related distress behavior at 12 months.
Standardized estimate Unstandardized estimate Z value P
Predictors FLACC 2 outcome
 FLACC 1 0.68 0.94 13.37 0.00
 PF 1 0.14 1.93 2.57 0.01
Parent Focused 2 outcome
 PF 1 0.53 0.65 6.98 0.00
 FLACC 1 0.01 0.00 0.18 0.86
FLACC 3 outcome
 FLACC 2 0.66 0.66 12.26 0.00
 PF 2 0.00 0.02 0.04 0.97
Parent Focused 3 outcome
 PF 2 0.67 0.66 10.00 0.00
 FLACC 2 0.03 0.00 0.42 0.68
FLACC is the measure of pain-related distress.
FLACC, Face, Legs, Activity, Cry, Consolability; PF, parent-focused.

Table 9 - Estimates for model of relationship between parent-focused behaviors and pain-related distress behavior at 18 months.
Standardized estimate Unstandardized estimate Z value P
Predictors FLACC 2 outcome
 FLACC 1 0.63 0.73 9.73 0.00
 PF 1 0.03 0.36 0.37 0.71
Parent Focused 2 outcome
 PF 1 0.63 0.63 9.67 0.00
 FLACC 1 0.07 0.01 1.02 0.31
FLACC 3 outcome
 FLACC 2 0.74 0.74 13.47 0.00
 PF 2 0.04 0.52 0.60 0.55
Parent Focused 3 outcome
 PF 2 0.62 0.69 9.85 0.00
 FLACC 2 −0.00 −0.00 −0.05 0.96
FLACC is the measure of pain-related distress.
FLACC, Face, Legs, Activity, Cry, Consolability; PF, parent-focused.

Table 10 - Estimates for model of relationship between physical self-soothing and pain-related distress behavior at 12 months.
Standardized estimate Unstandardized estimate Z value P
Predictors FLACC 2 outcome
 FLACC 1 0.70 0.97 14.43 0.00
 Self-Soothing 1 −0.00 −0.10 −0.07 0.95
Self-Soothing 2 outcome
 Self-Soothing 1 0.59 0.77 11.54 0.00
 FLACC 1 −0.12 −0.01 −1.66 0.10
FLACC 3 outcome
 FLACC 2 0.66 0.67 12.03 0.00
 Self-Soothing 2 0.01 0.10 0.09 0.93
Self-Soothing 3 outcome
 Self-Soothing 2 0.62 0.68 10.19 0.00
 FLACC 2 0.09 0.01 1.50 0.13
FLACC is the measure of pain-related distress. Self-soothing reflects physical self-soothing.
FLACC, Face, Legs, Activity, Cry, Consolability.

Table 11 - Estimates for model of relationship between physical self-soothing and pain-related distress behavior at 18 months.
Standardized estimate Unstandardized estimate Z value P
Predictors FLACC 2 outcome
 FLACC 1 0.62 0.71 10.77 0.00
 Self-Soothing 1 −0.12 −2.61 −1.92 0.05
Self-Soothing 2 outcome
 Self-Soothing 1 0.73 0.78 10.42 0.00
 FLACC 1 −0.01 −0.00 −0.09 0.93
FLACC 3 outcome
 FLACC 2 0.77 0.76 14.99 0.00
 Self-Soothing 2 0.05 1.01 0.84 0.40
Self-Soothing 3 outcome
 Self-Soothing 2 0.75 0.83 11.77 0.00
 FLACC 2 −0.07 −0.00 −1.17 0.24
FLACC is the measure of pain-related distress. Self-soothing reflects physical self-soothing.
FLACC, Face, Legs, Activity, Cry, Consolability.

Table 12 - Fit indices for models.
Model CFI TLI RMSEA
Disengagement of Attention—12 mo 1.00 1.05 0.00
Disengagement of Attention—18 mo 1.00 1.01 0.00
Parent-Focused—12 mo 1.00 0.99 0.03
Parent-Focused—18 mo 0.99 0.96 0.09
Physical Self-Soothing—12 mo 1.00 1.01 0.00
Physical Self-Soothing—18 mo 0.99 0.96 0.09
CFI, comparative fit index; RMSEA, root mean square error of approximation; TLI, Tucker–Lewis index.

3.2.1. Disengagement of attention at 12 months

As shown in Table 6 and Figure 2, across the 3 minutes postvaccination, use of disengagement of attention at each minute was significantly predicted by use of disengagement of attention in the previous minute (standardized βs = 0.36-0.49). The same pattern occurred with pain-related distress scores being predicted significantly by scores in the previous minute (standardized βs = 0.66-0.69). Use of disengagement of attention did not significantly predict subsequent pain-related distress responses in the post-vaccination period. Similarly, pain-related distress responses did not significantly predict subsequent use of disengagement of attention in the postvaccination period. There were no significant concurrent residual relations between use of disengagement of attention and pain-related distress behavior.

3.2.2. Disengagement of attention at 18 months

As shown in Table 7 and Figure 3, across the 3 minutes immediately postvaccination, use of disengagement of attention at each minute was significantly predicted by use of disengagement of attention in the previous minute (standardized βs = 0.36-0.60). The same pattern occurred with pain-related distress scores being predicted by scores in the previous minute (standardized βs = 0.64-0.74). Pain-related distress behavior at 1 minute postneedle (FLACC 1) significantly predicted less use of disengagement of attention at 2 minutes postneedle (Disengagement of Attention 2; standardized β = −0.23). No other predictive between-measure relations were significant. Finally, there was a significant concurrent negative relationship between use of disengagement of attention and pain-related distress behavior at 1 minute postneedle (residual r = −0.17). No other concurrent relations were significant.

3.2.3. Parent-focused strategies at 12 months

As shown in Table 8 and Figure 4, postvaccination, use of parent-focused emotion regulation behaviors at each minute was significantly predicted by use of parent-focused behaviors in the previous minute (standardized βs = 0.53-0.67). Pain-related distress behavior also significantly predicted subsequent pain-related distress (standardized βs = 0.66-0.68). Use of parent-focused emotion regulation behaviors at 1 minute postneedle (Parent Focused 1) significantly predicted more pain-related distress behavior at 2 minutes postneedle (FLACC 2; standardized β = 0.14). No other predictive between-measure relations were significant in this model. Finally, there was a significant positive concurrent relationship between use of parent-focused emotion regulation behaviors and pain-related distress behaviors at 3 minutes postneedle (Parent Focused 3 and FLACC 3; residual r = 0.20). No other concurrent relations were significant.

3.2.4. Parent-focused strategies at 18 months

As shown in Table 9 and Figure 5, use of parent-focused emotion regulation behaviors at each minute postvaccination was significantly predicted by use of parent-focused behaviors in the previous minute (standardized βs = 0.62-0.63). Pain-related distress behavior also significantly predicted subsequent pain-related distress (standardized βs = 0.63-0.74). Use of parent-focused emotion regulation behaviors did not significantly predict subsequent pain-related distress responses. Similarly, pain-related distress responses did not significantly predict subsequent use of parent-focused behaviors. There were significant positive concurrent relations between use of parent-focused emotion regulation behaviors and pain-related distress behavior at 1 minute postneedle (Parent Focused 1 and FLACC 1; residual r = 0.38) and 2 minutes postneedle (Parent Focused 2 and FLACC 2; residual r = 0.16). The residual relationship at 3 minutes postneedle was not significant.

3.2.5. Physical self-soothing strategies at 12 months

As shown in Table 10 and Figure 6, use of physical self-soothing significantly predicted use of physical self-soothing in subsequent minutes postvaccination (standardized βs = 0.59-0.62). Pain-related distress behavior also significantly predicted subsequent pain-related distress (standardized βs = 0.66-0.70). There were no significant predictive between-measure relations between use of physical self-soothing and pain-related distress. There were significant negative relations between use of physical self-soothing and pain-related distress behavior at 1 minute (Self-Soothing 1 and FLACC 1; residual r = −0.28) and 3 minutes postneedle (Self-Soothing 3 and FLACC 3; residual r = −0.19). The concurrent residual relationship at 2 minutes postneedle was not significant.

3.2.6. Physical self-soothing strategies at 18 months

As shown in Table 11 and Figure 7, use of physical self-soothing significantly predicted use of physical self-soothing in subsequent minutes postvaccination (standardized βs = 0.73-0.75). Pain-related distress behavior also predicted subsequent pain-related distress (standardized βs = 0.62-0.77). There were no significant predictive between-measure relations between use of physical self-soothing and pain-related distress. There was a significant negative relationship between use of physical self-soothing and pain-related distress behavior at 1 minute (Self-Soothing 1 and FLACC 1; residual r = −0.20). The concurrent residual relations at 2 and 3 minutes postneedle were not significant.

4. Discussion

The purpose of this study was to better understand child-led emotion regulation by assessing concurrent and predictive relations between child-led emotion regulation behaviors and pain-related distress in the vaccination context across the second year of life. The toddler period is a key developmental phase in emotion regulation skills25,26,40,41 and an ideal time to assess the emergence of these behaviors and their role in pain-related distress regulation.

Although it has been established in this cohort47 that, at both 12 and 18 months of age, pain-related distress at 1 minute postneedle predicted pain-related distress at subsequent minutes, novel relationships were elucidated in relation to the child-led emotion regulation behaviors. For all 3 child-led emotion regulation behaviors, behavior at 1 minute predicted behavior at subsequent minutes. Expanding on the known consistency in pain-related distress responses during toddler vaccinations,47 these results show that the more toddlers use these behaviors early in the appointment, the more they will use them later in the appointment. The next sections discuss the findings regarding the concurrent between-variable relations and the cross-lagged between-variable relations at both ages, across each of the 3 child-led regulatory behavior clusters.

4.1. The role of child-led disengagement of attention

At 12 months, there were no significant concurrent or predictive relations between disengagement of attention and pain-related distress. This finding suggests that this behavior may not yet serve a regulatory function at this age. In contrast, concurrent and predictive relations were seen at 18 months. Specifically, at 1 minute postneedle, there was a significant concurrent negative relationship between disengagement of attention and pain-related distress, which suggests that across the first minute after the needle, greater disengagement of attention is concurrently associated with less pain-related distress. Moreover, when assessing the predictive relations over time, more pain-related distress at 1 minute postneedle was related to less disengagement of attention the following minute. When children are highly distressed, it is difficult for them to engage with and explore their environment (eg, orienting toward or manipulating objects). Instead, this high distress is more likely to result in seeking comfort from a caregiver.5 It is important to understand that although some children may have explored their environment more, other children may have used objects their parents provided them initially to disengage their attention. If the parent was leading the distraction, this was not coded as “child-led.” Future work addressing child-led disengagement of attention strategies in the vaccination context could disentangle the multiple types of distraction that may be co-occurring as children age (ie, self-led vs parent-led).

4.2. The role of parent-focused behaviors

At 12 months, children's use of parent-focused behaviors at 1 minute postneedle predicted greater pain-related distress at 2 minutes postneedle, and there was a significant concurrent relationship between pain-related distress and parent-focused behaviors at 3 minutes postneedle. At 18 months, there were concurrent positive relations between parent-focused behaviors and pain-related distress at 1 and 2 minutes postneedle. In line with previous findings,20,39 the magnitude of the concurrent relations increased with age, which suggests that parent-focused behaviors may be more impactful as the attachment relationship develops.5 These positive relations may indicate that use of parent-focused behaviors do not reduce distress. However, this finding does not necessarily mean that this behavior is not regulatory or does not serve as a strategy for reducing pain. Indeed, these behaviors may serve as a signalling function to show caregivers that children need support. If so, it is not necessarily the act of seeking out their parent that supports distress regulation but rather that the high distress triggers signalling that in turn triggers parents to support pain-related distress regulation. Past research has shown that when parents respond to their children in a sensitive way, pain-related distress goes down,2,33 whereas when they use insensitive behaviors, distress increases.3,34

4.3. The role of physical self-soothing

At 12 months, we found significant negative concurrent relations between physical self-soothing and pain-related distress at 1 and 3 minutes postneedle. At 18 months, there was a negative concurrent relationship between physical self-soothing and pain-related distress at 1 minute postneedle. In contrast to the other 2 types of child-led emotion regulation behaviors, the magnitude of this association was lower at 18 months than at 12 month, which is consistent with the literature.20,39 Physical self-soothing may be a particularly helpful regulatory strategy in infancy and early toddlerhood for vaccination, but as the child continues to develop, physical strategies may be less useful, and children begin to rely on others. Like disengagement of attention, some of these strategies (eg, sucking on a pacifier) are connected to parent behavior (eg, the offering of a pacifier). It is important for researchers to demarcate parent pacifying (ie, placing the pacifier in mouth or holding it in) from self-directed self-soothing (ie, child keeping the pacifier in their own mouth). Future work is needed to address how parent soothing behaviors and child-led emotion regulation behaviors work together to promote a reduction in pain-related distress.

4.4. Limitations and future directions

These findings are understood within the context of some limitations. First, although culturally diverse, the current sample is primarily middle-class and highly educated; thus, these findings may not generalize to high-risk populations. Second, only observable behavior was used as an indicator of pain-related distress post-needle in the current analyses. Previous research has shown that behavioral and physiological indicators of pain may reflect different components of the pain experience,47 and thus, future research may set out to understand these relations with physiological distress indicators. Future research may also show how the relations between child-led regulatory behavior and pain behaviors develop as children begin to reach preschool age of 3 and 4 years. It is possible that providing information sheets to parents during the vaccination appointment may have influenced parent behavior and overall sensitivity during the vaccination appointment. This in turn may have influenced toddler signalling and use of parent-focused behaviors. But as a study focused on toddlers, we believe these indirect effects would not be strong enough to influence a toddler's use of regulatory behaviors.

5. Conclusions: implications for research and clinical practice

In conclusion, there is emerging evidence of the role of child-led pain-related distress regulation during the second year of life. Across 12 and 18 months, disengagement of attention and physical self-soothing strategies are related to decreased distress, whereas parent-focused behaviors are related to increased distress. In every model, a number of pathways were not significant reflecting that while toddlers' use of self-regulation is emerging, there are a number of other factors at play. This finding suggests that disengagement of attention and physical self-soothing may play more of a direct regulatory role, whereas parent-focused behaviors may play more of a signalling role, reflective of the child choosing to seek out parent support. Use of disengagement of attention and parent-focused behaviors show stronger relations with pain-related distress at 18 months, suggesting that these skills may be particularly relevant as children continue to develop. In contrast, weaker relations were seen between physical self-soothing behaviors and pain-related distress in older toddlers, suggesting that these emotion regulation strategies may become less useful as children develop.

Taken together, these findings show that emerging emotion regulation skills are seen in routine vaccination appointments. These findings have several research implications, and we recommend that researchers begin to measure both pain-related distress and child-led emotion regulation behaviors to fully understand the construct of regulation. These findings also suggest that toddlers are not passive participants in their routine vaccinations, wholly dependent on caregivers for distress regulation. As these findings do not negate the importance of parents and caregivers, they instead suggest a nuanced developmental interplay of child-led and parent-led regulation strategies interacting and evolving over time. These findings have substantial implications for knowledge translation efforts geared toward reducing pain in children. In conjunction with teaching parents what they can do to support their children's pain, helping them to support the development of independent child-led emotion regulation behaviors for vaccination may have implications for the development of confidence and agency in their own pain management and medical care.

Conflict of interest statement

The authors have no conflict of interest to declare.

Supplemental video content

A video abstract associated with this article can be found at https://links.lww.com/PAIN/B745.

Acknowledgements

The authors would like to acknowledge Dr. Jeffrey Gagne for his consultation support in modifying the Lab-TAB behaviors to the vaccination context. This work was funded by a Social Sciences and Humanities Research Council Doctoral Fellowship awarded to H. G. Gennis (752-2019-2734), a Natural Sciences and Engineering Research Council of Canada Discovery Grant (RGPIN-2016-06813), and a Canada Foundation for Innovation Grant (29908) awarded to R. R. Pillai Riddell. This work was also supported by a Lillian Meighen Wright Maternal Child Health Graduate Scholarship, the LaMarsh Centre for Child and Youth Research, and the Pain in Child Health Strategic Training Program (H. G. Gennis).

References

[1]. Anand KJ, Hickey RP. Pain and its effects in the human neonate and fetus. N Engl J Med 1987;21:1321–9.
[2]. Atkinson N, Gennis H, Racine N, Pillai Riddell R. Caregiver emotional availability, caregiver soothing behaviours, and infant pain during infant immunization. J Pediatr Psychol 2015;40:1105–14.
[3]. Badovinac S, Gennis H, Riddell RP, Garfield H, Greenberg S. Understanding the relative contributions of sensitive and insensitive parent behaviors on infant vaccination pain. Children 2018;5:80.
[4]. Blount RL, Devine KA, Cheng PS, Simons LE, Hayutin L. The impact of adult behaviors and vocalizations on infant distress during immunizations. J Pediatr Psychol 2008;33:1163–74.
[5]. Bowlby J. Attachment and loss. In: Attachment. Vol. 1. New York: Basic Books, 1969/1982.
[6]. Braungart JM, Stifter CA. Regulation of negative reactivity during the strange situation: temperament and attachment in 12-month-old infants. Infant Behav Develop 1991;14:349–64.
[7]. Braungart-Rieker J, Garwood MM, Powers BP, Notaro PC. Infant affect and affect regulation during the still-face paradigm with mothers and fathers: the role of infant characteristics and parental sensitivity. Develop Psychol 1998;34:1428–37.
[8]. Braungart-Rieker JM, Hill-Soderlund AL, Karrass J. Fear and anger reactivity trajectories from 4 to 16 months: the roles of temperament, regulation, and maternal sensitivity. Develop Psychol 2010;46:791–804.
[9]. Bridges LJ, Grolnick WS, Connell JP. Infant emotion regulation with mothers and fathers. Infant Behav Develop 1997;20:47–57.
[10]. Buss KA, Goldsmith HH. Fear and anger regulation in infancy effects on the temporal dynamics of affective expression. Child Develop 1998;69:359–74.
[11]. Campbell L, Riddell RP, Garfield H, Greenberg S. A cross-sectional examination of the relationships between caregiver proximal soothing and infant pain over the first year of life. PAIN 2013;154:813–23.
[12]. Campbell L, Pillai Riddell R, Cribbie R, Garfield H, Greenberg S. Preschool children's coping responses and outcomes in the vaccination context: child and caregiver transactional and longitudinal relationships. PAIN 2018;159:314–30.
[13]. Cole PM, Martin SE, Dennis TA. Emotion regulation as a scientific construct: methodological challenges and directions for child development research. Child Develop 2004;75:317–33.
[14]. Cole PM, Tan PZ, Hall SE, Zhang Y, Crnic KA, Blair CB, Li R. Developmental changes in anger expression and attention focus: learning to wait. Develop Psychol 2011;47:1078–89.
[15]. Ekas NV, Braungart-Rieker JM, Lickenbrock DM, Zentall SR, Maxwell SM. Toddler emotion regulation with mothers and fathers: temporal associations between negative affect and behavioral strategies. Infancy 2011;16:266–94.
[16]. Ekas NV, Braungart-Rieker JM, Messinger DS. The development of infant emotion regulation: time is of the essence. In: Cole PM, Hollenstein T, editors. Emotion regulation: a matter of time. New York: Routledge, 2013. p. 32–51.
[17]. Gagne JR, Van Hulle CA, Aksan N, Essex MJ, Goldsmith HH. Deriving childhood temperament measures from emotion-eliciting behavioral episodes: scale construction and initial validation. Psychol Assess 2011;23:337–53.
[18]. Geangu E, Benga O, Stahl D, Striano T. Individual differences in infants' emotional resonance to a peer in distress. Self-other awareness and emotion regulation. Soc Develop 2011;20:450–70.
[19]. Gennis H, Pillai Riddell R. Pain in infancy: the primacy of the social context. In: Prkachin K, Vervoort T, Trost Z, Karos KM, editors. Social and interpersonal dynamics of pain: we don't suffer alone. New York: Springer, 2018. p. 379–93.
[20]. Gennis HG, Bucsea O, Badovinac SD, Costa S, McMurtry CM, Flora DB, Pillai Riddell R. Child distress expression and regulation behaviors: a systematic review and meta-analysis. Children 2022;9:174.
[21]. Goldsmith HH, Rothbart MK. The laboratory temperament assessment battery (locomotor version). 3.1 ed. Wisconsin: University of Wisconsin-Madison.
[22]. Grolnick WS, Bridges LJ, Connell JP. Emotion regulation in two-year-olds: strategies and emotional expression in four contexts. Child Develop 1996;67:928–41.
[23]. Jahromi LB, Putnam SP, Stifter CA. Maternal regulation of infant reactivity from 2 to 6 months. Develop Psychol 2004;40:477–87.
[24]. Kessler RC, Greenberg DF. Linear panel analysis. New York: Academic Press, 1981.
[25]. Kopp CB. Antecedents of self-regulation: a developmental perspective. Develop Psychol 1982;18:199–214.
[26]. Kopp CB. Regulation of distress and negative emotions: a developmental view. Develop Psychol 1989;25:343–54.
[27]. Lewis M, Ramsay DS. Effect of maternal soothing on infant stress response. Child Develop 1999;70:11–20.
[28]. Lisi D, Campbell L, Riddell RP, Garfield H, Greenberg S. Naturalistic parental pain management during immunizations during the first year of life: observational norms from the OUCH cohort. PAIN 2013;154:1245–53.
[29]. Merkel SI, Voepel-Lewis T, Shayevitz JR, Malviya S. The FLACC: a behavioral scale for scoring postoperative pain in young children. Pediatr Nurs 1997;23:293–7.
[30]. Merkel S, Voepel-Lewis T, Malviya S. Pain assessment in infants and young children: the FLACC scale: a behavioral tool to measure pain in young children. Am J Nurs 2002;102:55–8.
[31]. Pillai Riddell R, Racine NM, Craig KD, Campbell L. Psychological theories and biopsychosocial models in pediatric pain. In: McGrath P, Stevens B, Walker S, Zempsky W, editors. The oxford textbook of pediatric pain. Oxford: Oxford University Press, 2013. p. 85–94.
[32]. Pillai Riddell RR, Racine NM, Gennis HG, Turcotte K, Uman LS, Horton RE, Ahola Kohut S, Hillgrove Stuart J, Stevens B, Lisi DM. Non-pharmacological management of infant and young child procedural pain (review). Cochrane Database Syst Rev 2015;12:1–198.
[33]. Pillai Riddell R, Campbell L, Flora DB, Racine N, Din Osmun L, Garfield H, Greenberg S. The relationship between caregiver sensitivity and infant pain behaviors across the first year of life. PAIN 2011;152:2819–26.
[34]. Pillai Riddell R, Gennis H, Tablon P, Greenberg S, Garfield H. Developing a measure of distress-promoting parent behaviors during infant vaccination: assessing reliability and validity. Can J Pain 2018;2:135–44.
[35]. Planalp EM, Van Hulle C, Gagne JR, Goldsmith HH. The infant version of the laboratory temperament assessment battery (Lab-TAB): measurement properties and implications for concepts of temperament. Front Psychol 2017;8:846.
[36]. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.470.5851&rep=rep1&type=pdf. Accessed February 26, 2021.
[37]. Rodkey EN, Pillai Riddell R. The infancy of infant pain research: the experimental origins of infant pain denial. J Pain 2013;14:338–50.
[38]. Rosseel Y. lavaan: an R package for structural equation modeling. J Stat Softw 2012;48:1–36.
[39]. Rothbart MK, Ziaie H, O'Boyle CG. Self-regulation and emotion in infancy. In: Eisenberg G, Fabes RA, editors. New directions for child development: the Jossey-Bass education series. San Francisco: Jossey-Bass Publishers, 1992. p. 7–23.
[40]. Sameroff A. A unified theory of development: a dialectic integration of nature and nurture. Child Develop 2010;81:6–22.
[41]. Sroufe LA. Emotional development: the organization of emotional life in the early years. New York, NY: Cambridge University Press, 1996.
[42]. Statistics Canada. Toronto—a data story on ethnocultural diversity and inclusion in Canada, 2019. Available at: https://www150.statcan.gc.ca/n1/pub/11-631-x/11-631-x2019002-eng.htm. Accessed July 24, 2022.
[43]. Stifter CA, Braungart JM. The regulation of negative reactivity in infancy: function and development. Develop Psychol 1995;31:448–55.
[44]. Taddio A, Appleton M, Bortolussi R, Chambers C, Dubey V, Halperin S, Hanrahan A, Ipp M, Lockett D, MacDonald N, Midmer D, Mousmanis P, Palda V, Pielak K, Riddell RP, Rieder M, Scott J, Shah V. Reducing the pain of childhood vaccination: an evidence-based clinical practice guideline. Can Med Assoc J 2010;182:E843–55.
[45]. Thompson RA. Emotion regulation: A theme in search of a definition. Monogr Soc Res Child Dev 1994;59:25–52.
[46]. Unruh AM, McGrath PJ. History of pain in children. In: Stevens BJ, Hathway G, Zempsky WT, editors. The oxford textbook of pediatric pain. 2nd ed. Oxford: Oxford University Press, 2021. p. 3–10.
[47]. Waxman JA, DiLorenzo MG, Pillai Riddell RR, Flora DB, Schmidt LA, Garfield H, Flanders D, Weinberg E, Savlov D. An examination of the reciprocal and concurrent relations between behavioral and cardiac indicators of acute pain in toddlerhood. PAIN 2020;161:1518–31.
Keywords:

Toddler; Acute pain; Vaccination; Self-regulation

Supplemental Digital Content

© 2023 International Association for the Study of Pain