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Journal of Pediatric Psychology logoLink to Journal of Pediatric Psychology
. 2024 Nov 23;50(4):307–316. doi: 10.1093/jpepsy/jsae095

Caregivers’ physiological responses during toddler vaccinations: associations with psychological and behavioral responses

Shaylea D Badovinac 1, David B Flora 2, Heather Edgell 3, Dan Flanders 4, Hartley Garfield 5,6, Eitan Weinberg 7, Deena Savlov 8, Rebecca R Pillai Riddell 9,10,11,✉
PMCID: PMC12013813  PMID: 39579363

Abstract

Objective

This study investigated biological, psychological, and behavioral aspects of caregivers’ responses to toddlers’ pain-related distress by measuring caregivers’ high-frequency heart rate variability (HRV) responses during toddler vaccination pain and examining associations with caregivers’ behavioral responses and psychological stress.

Methods

Participants included caregiver–toddler dyads (N = 194) from a longitudinal cohort-sequential study who were observed during toddlers’ 12-, 18-, or 24-month routine vaccinations. Changes in caregiver HRV were analyzed using growth curve modeling. Conditional growth curve models examined associations between caregiver HRV and caregivers’ concurrent behavior and psychological stress.

Results

The unconditional growth curve model indicated a slight linear decrease in caregiver HRV (i.e., vagal withdrawal) across the 3 min post-needle (unstandardized B = –0.06, p = .049). In conditional growth curve models, higher levels of parenting stress were associated with less vagal withdrawal during the post-needle period (standardized B = 0.47, unstandardized B = 0.02, p = .003). Caregivers’ behavioral responses (i.e., use of soothing and distress-promoting behaviors), state anxiety, and general anxiety symptomology were not significantly associated with HRV responses.

Conclusions

Caregiver parasympathetic nervous system activity levels changed minimally from baseline to post-needle and decreased slightly across the post-needle period. Caregivers’ self-reported parenting stress was associated with their parasympathetic responses to the procedure. Findings support an improved understanding of the mechanisms underlying caregivers’ responses to children’s pain-related distress in a naturalistic setting.

Keywords: acute pain, caregiver functioning, infancy and early childhood, parent psychosocial functioning, stress

 

Vaccinations are a common painful experience during early childhood (Centers for Disease Control and Prevention, 2023) and elicit moderate to high pain-related distress for most toddlers (Waxman et al., 2021). Although pain-related distress is typically brief, with most toddlers recovering within a few minutes of the needle, children who form distressing memories of painful procedures in early childhood are at an increased risk of long-term negative outcomes such as needle anxiety and avoidance of medical procedures (Kennedy et al., 2008).

The International Association for the Study of Pain’s conceptualization of pain emphasizes the influence of social factors on the experience of pain (Raja et al., 2020). In early childhood—a stage defined by emerging abilities to speak, self-regulate, and make sense of the world—children are highly influenced by the social context of their primary caregiver. Theory and longitudinal evidence suggest that caregivers’ responses to children’s pain reflect a complex interplay of biological, psychological, and social factors (Pillai Riddell et al., 2022). These include proximal influences, such as caregivers’ acute emotional state, pain management behaviors, and stress physiology, and distal factors, such as caregivers’ mental health and parenting experiences. However, the literature on the interplay of parental factors is sparse. The current study provides an in-depth analysis of caregivers’ physiological response to toddlers’ acute pain and examines relationships with caregivers’ behaviors and psychological stress.

Caregivers’ physiological responses to child pain and distress

Heart rate variability (HRV) is a commonly used physiological marker of caregivers’ physiological responses to their child’s distress (Badovinac et al., 2023a). High-frequency HRV reflects the activity of the parasympathetic branch of the autonomic nervous system. At rest, higher HRV indicates higher parasympathetic control, which serves a “brake” function on the heart. During acute stress, a decrease in HRV from baseline (i.e., vagal withdrawal) reflects an adaptive response to threat by supporting increased sympathetic and decreased parasympathetic nervous system activity for the purpose of threat management (Porges, 2007). Conversely, increased HRV from baseline is hypothesized to be adaptive in situations requiring social engagement by activating neural pathways involved in social behaviors (e.g., emotional expression, gaze, attention to human voice; Porges et al., 1994; Porges, 2007).

Most studies have investigated caregivers’ HRV responses to infants’ and toddlers’ distress in laboratory-based distress paradigms that elicit attachment-related fear by making the caregiver briefly unavailable to their infant or toddler (e.g., through physically separating the dyad or restricting the caregiver’s emotional responding to the child). Studies typically report a pattern of caregivers’ vagal withdrawal, relative to baseline, when caregivers reunite with and respond to their distressed infant (Busuito et al., 2019; Hill-Soderlund et al., 2008; Lan et al., 2022; Leerkes et al., 2017; Schechter et al., 2014). This suggests that caregivers experience children’s attachment-related distress as a threat to homeostasis requiring a shift in physiological resources to manage.

Research examining caregivers’ physiological responses to their children’s pain-related distress is limited (Badovinac et al., 2023a). Two studies of school-aged children found that caregivers exhibit vagal withdrawal while observing their child perform the Cold Pressor Task (Constantin et al., 2022a; Vervoort et al., 2014), suggesting that pain-related laboratory-based distress tasks evoke similar physiological responses in caregivers as other laboratory-based distress tasks. However, these findings may not generalize to naturalistic contexts, which differ in that they do not constrain caregivers’ availability to respond to their child’s distress and they involve a degree of uncontrollability for caregivers (as procedural pain, unlike separation distress, cannot be instantaneously discontinued). Painful procedures such as routine vaccination provide a context to study caregivers’ naturalistic physiological and behavioral responses in a situation that more closely approximates the caregiving demands of everyday life.

The first study of caregivers’ physiological responses to toddlers’ pain-related distress discerned groups of caregiver–toddler dyads based on HRV attunement patterns during routine vaccination (Di Lorenzo-Klas et al., 2023a). Within most dyads, caregivers showed relatively stable HRV levels from baseline to three minutes post-needle. Although this study focused on identifying trajectories of dyadic responding (as opposed to specifically caregivers’ responding), it prompts a question of the factors that contribute to individual differences in caregivers’ HRV responses. The only other study of caregivers’ HRV during procedural pain focused on caregivers of school-aged children undergoing venipuncture (Constantin et al., 2022b) and found decreases in caregivers’ HRV pre-, during, and post-venipuncture, relative to a resting baseline.

Associations between caregivers’ physiological, psychological, and behavioral responses to children’s pain-related distress

A notable gap in the literature concerns how caregivers’ physiological responses relate to psychological and behavioral aspects of caregivers’ responses. Within the pain context, there is mixed evidence for associations between caregivers’ state anxiety (i.e., self-report of their psychological stress during their child’s pain) and physiological responding. One study found that caregivers who self-report higher pre-needle and lower post-needle state anxiety exhibit less adaptive co-regulatory patterns with their toddlers during vaccination (DiLorenzo-Klas et al., 2023b); however, other research has found caregivers’ state anxiety to be minimally associated (r’s = –.13–0) with HRV reactivity during venipuncture in school-aged children (Constantin et al., 2022b).

To date, no studies have examined how caregivers’ physiological responses relate to their concurrent soothing behaviors in response to their infants or toddlers’ pain. In other toddler distress contexts, higher average caregiver HRV during toddlers’ distress and increased HRV from baseline in response to toddlers’ distress have been associated with caregivers’ use of fewer over-reactive discipline strategies (Lorber & O’Leary, 2005) and other negative parenting behaviors (e.g., criticism; Miller et al., 2015). In contrast, among caregivers of school-aged children, lower caregiver HRV has been associated with greater use of coping-promoting behaviors (e.g., child-directed humor, non-procedure related talk, encouragement of coping) and not associated with their use of distress-promoting behaviors (e.g., criticism, verbal reassurance, apology; Constantin et al., 2022a) during the Cold Pressor Task.

Inconsistencies in the operationalization of HRV responses are a challenge across psychophysiological research that potentially contribute to mixed findings across studies (Beauchaine, 2001). Many studies define HRV reactivity as changes (i.e., difference scores) in average HRV levels between baseline and the various phases of a distress task. While difference scores denote the direction and magnitude of change in HRV elicited by a stressor, they do not capture the dynamics of change throughout the stressor, including the recovery trajectory. Moving beyond difference scores and using statistical approaches that characterize the direction, magnitude, and trajectory of HRV responses across time can offer insight into individual differences in HRV responses and how they relate to other aspects of individuals’ emotional and behavioral responses.

The current study

Caregivers who respond to their child’s pain with more sensitive behavior and less insensitive behavior have children who are better able to regulate pain (for a review, see Samdan et al., 2020), yet less is known about what underlies caregivers’ use of appropriate and inappropriate soothing behaviors. Examining caregivers’ physiological responses to child pain and their relation to caregivers’ behaviors and self-reported stress is therefore an important area of research. To our knowledge, the current study is the first to characterize the dynamics of caregivers’ HRV responses and associations with caregiver behavioral and psychological responses during vaccination pain.

Aim 1 was to characterize caregivers’ physiological response to toddlers’ pain-related distress during vaccination. This aim was first addressed in preliminary analyses that examined the direction and magnitude of change in average HRV from baseline to post-stressor, based on standardized mean differences, to facilitate comparison of our results to previous studies using this approach. We hypothesized that caregivers would exhibit a pattern of decreased HRV (i.e., vagal withdrawal) from baseline to post-stressor. Next, we used growth curve modeling to examine the trajectory of HRV responses throughout the stressor (i.e., across the post-needle period). Growth curve modeling involves the specification of latent variables representing the magnitude of caregivers’ initial HRV (i.e., HRV intercept latent variable) and the change in caregivers’ HRV responses across the post-needle period (i.e., HRV slope latent variable). We hypothesized that caregivers would exhibit the lowest HRV levels immediately after the needle (i.e., when toddlers exhibit the highest levels of pain-related distress) and an overall pattern of increasing HRV throughout the 3 min post-needle (i.e., positive HRV slope latent variable), corresponding with toddlers’ recovery from pain-related distress.

Aim 2 was to examine how caregivers’ physiological responses—represented by the HRV intercept and slope from Aim 1—relate to caregivers’ concurrent behavior and psychological stress. Behavior was defined in terms of caregivers’ use of soothing behaviors and distress-promoting behaviors, and psychological stress was characterized in terms of caregivers’ state anxiety (i.e., anxiety reported during the vaccination appointment) and general stress levels (i.e., self-reported parenting stress and anxiety symptoms for the 2 weeks surrounding the appointment). We hypothesized that lower caregiver HRV during the initial reactivity and early regulation phase of caregivers’ response (i.e., lower HRV intercept) and slower regulation of HRV (i.e., smaller increases in HRV slope) would relate to less optimal behavioral and psychological responses, including fewer soothing behaviors, more distress-promoting behaviors, and higher levels of state anxiety, parenting stress, and anxiety symptoms.

Methods

Participants

Participants were drawn from a larger longitudinal cohort-sequential study (N = 234) that followed healthy, typically developing toddlers and their caregivers during routine vaccination appointments across the second year of life (12, 18, and 24 months; see Di Lorenzo-Klas et al. [2023a] for further details). This study used a subsample of 194 caregiver–toddler dyads with physiological data available. For dyads with data available at multiple time points, only the final participation point was included in the current analyses to support a more even age distribution. Caregiver age, education, relation to child, and ethnicity and toddler sex were not significantly associated with dyads’ participation at a single (vs. multiple) time points, based on point-biserial correlations and chi-square tests (p’s > .05).

In the analyzed sample (N = 194), toddlers (54% male) were on average 18 months old (M = 17.6, SD = 4.4). Caregivers ranged in age from 20 to 62 years (M = 36, SD = 5.2) and were primarily mothers (81%), but also included fathers (18%) and grandparents (1%). Caregivers reflected a high level of educational attainment (47% completed graduate school or professional training, 37% attended or graduated university, 15% attended trade school or community college, and 1% had completed a high school education) and diverse self-reported heritage cultures (24% North American, 27% European origins, 23% Asian origins, 4% Latin, Central, or South American origins, 1% African origins, 1% Caribbean origins, 1% Oceanian origins, 8% other ethnic/cultural origins, and 12% mixed origins).1

Procedure

Ethical approval was obtained from the Research Ethics Board at York University. Caregivers of toddlers scheduled for a vaccination appointment were made aware of the study upon entering the pediatric clinic. Interested caregivers completed screening for inclusion and exclusion criteria (see Di Lorenzo-Klas et al., 2023a), and written informed consent was obtained from caregivers who agreed to participate. Recruitment and data collection occurred between December 2015 and December 2019 by research assistants who were blinded to the study hypotheses.

Caregiver–toddler dyads were videorecorded during the appointment and wore MindWare wireless ambulatory monitors (MW1000A), which recorded electrocardiography (ECG) data at a sampling rate of 500 Hz. Three ECG electrodes were placed on each caregiver and toddler, including one placed over the right clavicle, one under the bottom left rib, and one ground electrode under the bottom right rib. MindWare Biolab software (version 3.3) was used for continuous ECG acquisition and The Observer XT software synchronized video and cardiac data capture. Video and cardiac data were collected for 2 min before the vaccination needle and up to 5 min after the vaccination needle. Caregivers self-rated their own worry at the beginning and the end of the recording period. Once ECG monitoring equipment was in place, dyads were observed with minimal interference from the research team. As per standard clinical practice in the participating clinics, all caregivers held their toddler during the vaccination. Caregivers’ movement was unimpeded by the wireless ECG monitoring equipment. However, given the small size of the clinic rooms, caregivers did not move around significantly during the appointment. One percent of caregivers reported administering a topical anesthetic (e.g., EMLA) to toddlers prior to the appointment. At the end of the appointment, caregivers received a pamphlet on evidence-based pain management strategies. Following the appointment, caregivers were administered measures of self-reported general psychological distress and parenting stress over the phone. Most caregivers (i.e., 70%) completed phone measures within 3 weeks of the appointment. Processing and coding of data were completed in the lab using The Observer XT software and MindWare HRV software (version 3.1.5) by separate coding teams who were blinded to participant data on other measures and were unaware of the study hypotheses.

The current analysis involves caregiver physiological responses, soothing behavior, and psychological stress (i.e., self-reported anxiety and parenting stress). Previous studies of this cohort have reported on toddlers’ self-regulatory behaviors (Gennis et al., 2023) and behavioral and physiological reactivity (Waxman et al., 2020, 2021) and caregiver–toddler physiological attunement (Di Lorenzo-Klas et al., 2023a, 2023b).

Measures

Caregiver high-frequency HRV

ECG data were edited using MindWare HRV 3.1.5 software, which derived caregiver high-frequency HRV based on spectral analysis of RR intervals (i.e., the intervals between successive heart beats or R waves; Berntson et al., 1997) using frequency bands within the range of spontaneous respiration for adults (0.12–0.40; Cacioppo et al., 2000). Manual data inspection and artifact editing was conducted by three coders who were trained by an experienced graduate student primary coder. Artifact editing (e.g., due to software misidentification or equipment malfunction) occurred in consultation with the primary coder and impacted less than 5% of data for all participants. Interrater reliability with the primary coder, calculated on a randomly selected 20% of the sample, indicated strong reliability (intraclass correlations [ICC] from 0.96 to 0.99). Caregiver HRV was calculated for consecutive 30-s epochs during the minute before the vaccination needle (i.e., baseline) and 3 min post-needle, which were then averaged within each minute to yield average HRV during Baseline, and 1 min (Post 1), 2 min (Post 2), and 3 min post-needle (Post 3). All analyses included caregiver posture (i.e., percentage of time spent standing, coded concurrently from video footage) as a covariate due to its influence on HRV levels (Berntson et al., 2016).

Caregiver pre- and post-needle state anxiety

Caregivers rated their state anxiety on two occasions—once prior to the toddler’s needle and again approximately 3 min after the needle—by verbally responding to the question: “How worried are you right now on a scale of 1 to 10, where 1 is ‘no worry at all’ and 10 is ‘the most worry possible’?”, asked by a research assistant. Higher scores reflect more state anxiety. Subjective ratings of distress have been previously validated as a measure of acute emotional discomfort (Tanner, 2012).

Caregiver anxiety symptoms

Caregivers’ anxiety symptoms were self-reported using the anxiety scale of the Brief Symptom Inventory (BSI), a 53-item questionnaire used to evaluate psychological distress that has been validated in clinical and non-clinical adult populations (Derogatis & Melisaratos, 1983). T-scores are reported (i.e., standardized scores based on population mean = 50 and SD = 10), with higher scores on the anxiety scale reflecting more intense recent symptoms of anxiety.

Parenting stress

Caregivers completed the Parenting Stress Index—Fourth Edition, Short Form (PSI-4-SF; Abidin, 1995), a 36-item questionnaire used to evaluate stress related to the parent–child relationship. It consists of three subscales including parental distress (i.e., feelings of burden, distress, and support associated with the parenting role), parent–child dysfunctional interaction (i.e., extent to which interactions with child are rewarding or stressful), and difficult child (i.e., perception of child as having a difficult temperament). Subscale scores are combined to generate the Total Stress Index T-score, used in the current study, with higher scores reflecting more parenting stress.

Caregiver soothing behaviors

Caregiver soothing behaviors were coded from video footage of vaccination appointments using the Measure of Adult and Infant Soothing and Distress (MAISD; Cohen et al., 2005). Four soothing behaviors were analyzed, including distraction (i.e., directing child’s attention elsewhere by making faces, pointing, etc.), physical comfort (i.e., rubbing, patting, or massaging child), rocking (i.e., swaying or bouncing child), and verbal reassurance (e.g., making reassuring comments to child such as “it’s ok”). Each behavior was coded as present or absent during 5-s epochs throughout the 3 min post-needle. Proportion scores, ranging from 0 to 1 and reflecting the proportion of epochs during which the behavior was observed out of all codable epochs, were calculated. Higher scores reflect more frequent use of the soothing behavior across the 3 min post-needle. Coding was conducted by three undergraduate coders who were trained by an experienced primary coder. Interrater reliability, calculated as single-measures ICCs based on a randomly selected 20% of videos coded by the primary coder, ranged from 0.8 to 0.93 for physical comfort, 0.96 to 0.99 for rocking, and 0.81 to 0.95 for verbal reassurance.

Caregiver distress-promoting behaviors

Caregiver distress-promoting behaviors were coded from video footage of vaccination appointments using the Opportunities to Understand Childhood Hurt’s Inoculation Evaluation—Research Version (OUCHIE-RV; Badovinac et al., 2023b). The OUCHIE-RV codes caregivers’ use of three domains of distress-promoting behavior in response to child distress, including affect incongruence (e.g., verbal or non-verbal behaviors reflecting non-attuned affect, such as fearful, angry, overly positive, and/or restricted affect), attention diversion (i.e., attending away from distressed child, such as by speaking with someone else in the room), and physical distance (i.e., lapses in physical contact between caregiver and distressed child, such as putting down the distressed child). Each behavior domain was rated on a 0–2 scale during 30-s epochs spanning 3 minutes post-needle. Scores across behaviors and epochs were averaged, resulting in an overall OUCHIE-RV composite score representing distress-promoting behavior during the 3 min post-needle. Composite scores range from 0 to 2 and higher scores indicate more frequent or intense use of distress-promoting behavior in response to toddler distress. Coding was conducted by two undergraduate coders who were trained by an experienced graduate student primary coder. Interrater reliability, calculated as single-measures ICCs based on a randomly selected 20% of videos coded by the primary coder, ranged from 0.77 to 0.85.

Analysis plan

Preliminary analyses included the calculation of descriptive statistics and correlations among primary variables. Missing data rates were calculated and demographic factors potentially associated with missing data were examined using point-biserial correlations and chi-square tests.

To address Aim 1, we first examined the direction and magnitude of change in HRV from Baseline through Post 3 through calculation of standardized mean differences (Cohen’s d). Next, unconditional growth curve models (Bollen & Curran, 2006) were used to characterize the mean and variability of caregivers’ HRV during the first minute post-needle (i.e., initial reactivity and early regulation of HRV, reflected by the intercept latent variable) and the mean and variability of caregivers’ HRV across the three minutes post-needle (i.e., regulatory trajectory of HRV, reflected by the slope latent variable). The unconditional growth model modeled the linear change in HRV across the 3 min post-needle (i.e., Post 1, Post 2, and Post 3). The Tucker–Lewis Index (TLI), Comparative Fit Index (CFI), root mean square error of approximation (RMSEA), and standardized root mean squared residual (SRMR) were used to assess model fit (Bollen & Curran, 2006).

To address Aim 2, conditional models were estimated, which involves regressing the intercept and slope latent variables onto predictor variables, allowing for an examination of how caregivers’ initial reactivity and early regulation (intercept) and regulatory trajectories (slope) in HRV relate to other aspects of caregivers’ behavioral and psychological responses. Two conditional growth curve models were estimated. Model 1 examined how caregivers’ concurrent behavioral responses (i.e., behavior during the 3 min post-needle) predicted the HRV intercept and slope latent variables; the predictors included were distraction, physical comfort, rocking, verbal reassurance, and distress-promoting behaviors. Model 2 examined how caregiver stress variables predicted the HRV intercept and slope latent variables; the predictors included were caregivers’ pre-needle worry rating, post-needle worry rating, anxiety symptoms, and parenting stress. Both models included caregivers’ posture (i.e., percentage of time spent in a standing position) and baseline (i.e., pre-needle) HRV as covariates of the HRV intercept and slope latent variables.

Growth curve models were estimated in R (R Core Team, 2022) using the lavaan package (Rosseel, 2012). Robust maximum likelihood estimation was used, which allows for the inclusion of incomplete cases and produces model fit statistics and standard error estimates that are robust to non-normality. Alpha = .05 was used for all statistical tests.

Results

Descriptive statistics and preliminary analyses

Variables were approximately normally distributed, except Distraction, which showed significant positive skew. Distraction was thus dichotomized such that scores of 0 reflected no use of distraction and scores of 1 reflected any use of distraction. Rates of missing data ranged from 0.5% to 14.9% across variables. Missingness was not significantly associated with caregiver age, education, relation to child, ethnicity, or child sex, based on chi-square tests and point-biserial correlations (p > .05).

Descriptive statistics and correlations among primary variables are in Table 1. Caregivers reported relatively low levels of pre-needle and post-needle worry and normative levels of anxiety symptoms and parenting stress. Sample mean HRV levels reflected negligible increases in HRV from baseline to Post 1 (d = 0.08) and negligible decreases from Post 1 to Post 2 (d = –0.09) and from Post 2 to Post 3 (d = –0.03). Caregiver posture was significantly correlated with HRV at Post 1, Post 2, and Post 3 (r = –.25 to –.14, p < .05) and parenting stress was significantly correlated with HRV at Post 3 (r = .17, p < .05). HRV was not significantly correlated with caregiver age or sex (p>.05).

Table 1.

Descriptive statistics and correlations among study variables (n = 194).

n Mean (SD) or % Range 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13.
1. High-frequency HRV Base 183 4.74 (1.22) 1.1–9.16
2. High-frequency HRV Post 1 186 4.84 (1.22) 1.73–7.46 .57*
3. High-frequency HRV Post 2 186 4.73 (1.22) 1.99–8.06 .55* .73*
4. High-frequency HRV Post 3 186 4.69 (1.18) 1.74–7.74 .58* .74* .78*
5. Posture (time standing) 190 68.33 (43.75) 0–100 –.14 –.23* –.25* –.24*
6. Distraction 189 34.4a – .06 –.01 –.13 –.01 .16*
7. Physical comfort 189 0.45 (0.24) 0–1 –.08 .01 –.03 –.02 .01 –.05
8. Rocking 189 0.31 (0.31) 0–1 –.09 –.12 –.13 –.13 .47* .05 .27*
9. Verbal reassurance 188 0.14 (0.14) 0–0.61 .08 .01 .003 .02 .03 .23* .16* .09
10. Distress-promoting behavior 174 0.74 (0.4) 0–1.75 .06 –.03 .02 –.03 .03 .21* –.36* –.19* .05
11. Pre-needle state anxiety 191 2.5 (2.52) 0–10 .03 .08 .13 .1 –.01 –.04 .1 .04 .06 .002
12. Post-needle state anxiety 193 1.91 (2.39) 0–9 .11 .09 .1 .08 .1 .08 .12 .11 .05 –.03 .52*
13. Anxiety symptoms 168 47.77 (8.97) 38–71 .11 .11 .05 .12 .03 .04 –.09 –.1 –.08 .04 .16* .02
14. Parenting stress 167 43.9 (6.72) 33–65 .08 –.01 .08 .17* –.01 –.08 –.02 .02 –.07 –.05 .25* .13 .35*
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Note. HRV = high-frequency heart rate variability; Base = baseline.

a

Percentage reported (i.e., percentage of caregivers who used distraction).

*

p < .05.

Unconditional growth curve model

A linear growth model of caregiver post-needle HRV provided a good fit to the data (CFI = 1.00; TLI = 1.01; RMSEA = 0.00; SRMR = 0.01). Caregiver HRV slightly decreased from Post 1 to Post 3 (unstandardized mean of slope latent factor = –0.06, p = .049), reflecting a general trend of vagal withdrawal from Post 1 to Post 3. Variance estimates suggested substantial inter-individual variability in the level of HRV at Post 1 (intercept latent variable variance = 1.12, p < .001) and non-significant variability in the amount of HRV change from Post 1 to Post 3 (slope latent variable variance = 0.05, p = .41). Model estimates are in Table 2.

Table 2.

Unconditional growth curve model for caregiver high-frequency heart rate variability (HRV; N = 189).

Variable Unstandardized estimate SE Z p
Intercept latent variable
 Mean 4.82 0.09 54.92 <.001
 Variance 1.12 0.16 6.89 <.001
Slope latent variable
 Mean −0.06 0.03 –1.97 .049
 Variance 0.05 0.06 0.83 0.41
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Note. Comparative Fit Index = 1.00, Tucker–Lewis Index = 1.01, root mean square error of approximation = 0.00, standardized root mean squared residual = 0.008.

Conditional growth curve models

Model 1: Behavioral responses across the vaccination

Estimates for the conditional growth curve model of caregiver HRV and behavioral responses post-needle are in Table 3. Caregivers’ baseline HRV and posture were included as covariates. Baseline HRV was significantly positively associated with the HRV intercept latent variable (standardized B = 0.63, unstandardized B = 0.54, p < .001) but not the HRV slope (standardized B = –0.02, unstandardized B = –0.004, p = .91). The HRV intercept and slope latent variables were not significantly associated with caregiver posture or caregivers’ behavioral responses during the post-needle period (Table 3).

Table 3.

Conditional growth curve model examining associations between caregiver high-frequency heart rate variability (HRV) intercept and slope and caregivers’ behaviors during the 3 min post-needle (Model 1; N = 160).

Predictor Standardized estimate Unstandardized estimate SE Z p
Intercept
 Baseline HRV 0.63 0.54 0.08 6.74 <.001
 Posture –0.11 –0.003 0.002 –1.4 0.16
 Distraction –0.1 –0.2 0.19 –1.1 0.27
 Physical comfort 0.08 0.33 0.35 0.93 0.35
 Rocking 0.002 0.01 0.29 0.03 0.98
 Verbal reassurance –0.03 –0.22 0.7 –0.32 0.75
 Distress-promoting behavior 0.003 0.01 0.2 0.04 0.97
Slope
 Baseline HRV –0.02 –0.004 0.03 –0.11 0.91
 Posture 0.01 0 0.001 0.05 0.96
 Distraction 0.14 0.07 0.07 1 0.32
 Physical comfort –0.03 –0.03 0.15 –0.19 0.85
 Rocking –0.13 –0.11 0.12 –0.88 0.38
 Verbal reassurance –0.03 –0.05 0.24 –0.21 0.84
 Distress-promoting behavior –0.06 –0.04 0.08 –0.5 0.62
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Note. Comparative Fit Index = 1.00, Tucker–Lewis Index = 1.00, root mean square error of approximation = 0.00, standardized root mean squared residual = 0.01. Significant predictors (p < .05) are bolded.

Model 2: Caregiver stress

Estimates for the conditional growth curve model of caregiver HRV and caregiver stress variables are in Table 4. As in Model 1, caregivers’ baseline HRV remained significantly positively associated with the HRV intercept latent variable (standardized B = 0.62, unstandardized B = 0.51, p < .001) but not the HRV slope (standardized B = –0.03, unstandardized B = –0.01, p = .88). Caregiver posture was significantly associated with the HRV intercept latent variable (standardized B = –0.18, unstandardized B = –0.004, p = .01) but not the HRV slope (standardized B = 0.01, unstandardized B = 0.00, p = .95). Parenting stress was significantly positively associated with the HRV slope latent variable (standardized B = 0.47, unstandardized B = 0.02, p = .003), indicating that caregivers who reported higher levels of parenting stress showed less vagal withdrawal across the post-needle period. Finally, caregiver worry ratings and anxiety scores did not have significant unique associations with the HRV intercept or slope latent variables (Table 4).

Table 4.

Conditional growth curve model examining associations between caregiver high-frequency heart rate variability (HRV) intercept and slope and caregiver stress variables (Model 2; N = 151).

Predictor Standardized estimate Unstandardized estimate SE Z p
Intercept
 Baseline HRV 0.62 0.51 0.07 7.17 <.001
 Posture –0.18 –0.004 0.002 –2.52 0.01
 Worry Rating Pre-Needle 0.02 0.01 0.04 0.2 0.84
 Worry Rating Post-Needle 0.05 0.02 0.04 0.6 0.55
 Anxiety symptoms 0.07 0.01 0.01 1.00 0.32
 Parenting stress –0.1 –0.02 0.01 –1.34 0.18
Slope
 Baseline HRV –0.03 –0.01 0.03 –0.16 0.88
 Posture 0.01 0 0.001 –0.06 0.95
 Worry Rating Pre-Needle 0.11 0.01 0.02 0.65 0.52
 Worry Rating Post-Needle –0.06 –0.01 0.02 –0.29 0.77
 Anxiety symptoms –0.16 –0.004 0.004 –1.13 0.26
 Parenting stress 0.47 0.02 0.01 3.00 0.003
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Note. Confirmatory Factor Index = 1.00, Tucker–Lewis Index = 1.01, root mean square error of approximation = 0.00, standardized root mean squared residual = 0.01. Significant predictors (p < .05) are bolded.

Discussion

For the first time in the literature, this study investigated relationships between caregivers’ physiological responding to their toddlers’ vaccination and both their behavioral responses and self-reported stress. We characterized caregivers’ HRV responses in terms of the direction and magnitude of change from baseline and the trajectory of caregivers’ HRV responses during toddler vaccination (Aim 1) and examined concurrent associations between caregivers’ HRV responses (i.e., initial reactivity and early regulation of HRV and regulatory trajectories of HRV) and their behavior and self-reported stress (Aim 2).

Aim 1 elucidated caregivers’ HRV responses during toddlers’ pain-related distress. Preliminary analyses characterized the direction and magnitude of change from pre- to post-needle based on the standardized mean difference in HRV from Baseline to Post 1, with results indicating negligible changes (d = 0.08). Next, the intercept and slope of caregivers’ HRV responses across the post-needle period—reflecting caregivers’ initial reactivity and early regulatory trajectory of HRV—were examined using growth curve modeling. A linear growth model fit the data well and reflected a slight decrease in caregiver HRV from the early to late phases of toddlers’ pain-related distress. These findings did not support hypotheses, as we had expected a pattern of vagal withdrawal from baseline to post-needle and a trend of increasing caregiver HRV across the 3 min post-needle corresponding with toddlers’ recovery from pain-related distress.

The finding of minimally fluctuating caregiver HRV from baseline in response to toddlers’ distress is discrepant from previous studies, which have reported vagal withdrawal in response to children’s attachment-related distress (Busuito et al., 2019; Hill-Soderlund et al., 2008; Lan et al., 2022; Leerkes et al., 2017; Schechter et al., 2014) and pain-related distress (Constantin et al., 2022a, 2022b; Vervoort et al., 2014). Two factors may explain this discrepancy. First, previous studies in a pain context have compared caregivers’ HRV reactivity to a resting or low-demand baseline condition during which caregivers were not interacting with their child (Constantin et al., 2022a, 2022b; Vervoort et al., 2014). In comparison, baseline data in this study were collected during the minute before the needle, during which caregivers could interact freely with their toddler. Demands for social interaction during the pre-needle period in combination with the possibility that caregivers were coping with anticipatory distress (their own and/or their child’s) related to the needle may have contributed to a stress response in caregivers that preceded their child’s pain. This interpretation is supported by previous research showing that parents’ state anxiety during their child’s pain is more strongly associated with parents’ ratings of their child’s anticipatory distress than their pain-related distress (Kaluza et al., 2021). Thus, a longer period of baseline data collection may have been needed to capture the onset of caregivers’ stress response.

A second potential explanation is that the demands on caregivers within the context of vaccination are different from other distress contexts. During attachment stressors—which comprise most prior research—because the caregiver’s unavailability is the cause of the distress, the caregiver’s re-engagement with the child would be expected to lead to a prompt resolution of the child’s distress and return to normal caregiver–child interaction (Badovinac et al., 2023a). During vaccination, because the child’s pain persists even after the removal of the needle, there is a greater demand on caregivers to attune to their child’s distress behaviors, attempt various soothing behaviors, and monitor the child’s response to soothing behaviors in order to regulate the child’s distress. Maintaining stable HRV levels throughout the onset and course of toddler distress may support the ongoing social engagement behaviors (Porges, 2003) needed to maintain toddlers’ gaze and decode their evolving distress levels by attending to toddlers’ vocalizations and facial expression.

Aim 2 contextualized caregivers’ HRV responses with their concurrent behavioral responses and psychological stress. Conditional growth curve models examined how behavioral and psychological variables related to the HRV intercept (initial reactivity and early regulatory response post-needle) and slope (change over the 3 min post-needle) latent variables, while controlling for caregivers’ baseline HRV levels and posture. Contrary to hypotheses, associations between caregivers’ HRV responses and their concurrent use of soothing behaviors or distress-promoting behaviors were non-significant. Only one previous study examined associations between caregivers’ HRV levels and their concurrent use of soothing behaviors in a pain context; this study found a negative correlation between caregivers’ use of coping-promoting behaviors and their concurrent HRV levels during a Cold Pressor Task (Constantin et al., 2022a). In our results, of the caregiver behavior variables examined, rocking had the strongest correlations with caregiver HRV (r = –.12 to –.13; see Table 1) but was not significantly associated with the HRV intercept or slope latent variables alongside other aspects of soothing and distress-promoting behaviors in the conditional growth curve model. Caregivers’ behavioral responses and the influences underlying these responses are hypothesized to be multifactorial and complex, with different combinations of soothing and distress-promoting behaviors emerging from nuanced underlying emotional, cognitive, and physiological processes (Brown et al., 2018; Pillai Riddell et al., 2022). While our results are consistent with previous evidence for a pattern of negative relationships between caregivers’ parasympathetic activity levels and their use of soothing behaviors during child distress (Constantin et al., 2022a), the small correlations and non-significant growth curve model findings suggest that there are likely other important influences and interactions that should be considered concurrently within the model (e.g., using path analysis; Campbell et al., 2018) to support a more complete understanding of physiology–behavior associations.

The final conditional growth curve model examined associations between caregivers’ HRV responses and self-reported stress, including state anxiety during the vaccination and recent anxiety and stress symptoms as assessed by the BSI and the PSI, while controlling for baseline HRV levels and posture. Results provided partial support for hypotheses. Although caregivers’ state anxiety and recent anxiety symptoms were not significantly associated with the HRV intercept or slope latent variables, parenting stress was significantly associated with the HRV slope latent variable. Specifically, caregivers who reported higher levels of parenting stress exhibited less vagal withdrawal over the course of the post-needle period. One possible explanation for this finding is that caregivers with higher levels of parenting stress needed to maintain higher HRV levels across the post-needle period as a self-regulatory effort to deal with their child’s ongoing distress (Beauchaine, 2001). Higher parenting stress levels may ensue from having a child with more negative emotionality and who is less easily soothed, therefore requiring more active engagement and soothing from their caregiver, particularly during times of distress. However, it is also possible that, due to higher chronic stress levels, these caregivers have less of a “stress reserve” available to activate a stress response (e.g., vagal withdrawal) during their child’s distress. To further explore this hypothesis, future work could investigate how individual differences in caregiver stress and physiology relate to toddlers’ temperament and pain-related distress behavior.

Based on our findings, clinicians working with infants and young children should consider how caregivers’ anticipatory stress and chronic stress may impact on caregivers’ ability to engage in the medical appointment and respond appropriately to their child’s pain-related distress. Clinicians should be alert to behavioral indicators of elevated caregiver stress and anxiety, be prepared to offer evidence-based strategies for managing parents’ state anxiety (e.g., parental education; Santapuram et al., 2021), and consider when follow-up evaluation or referral to a mental health professional may be warranted.

Limitations

Owing to practical constraints of conducting research in a primary care setting, our baseline physiological data—collected over the 2 min pre-needle and analyzed for the minute immediately preceding the needle—do not reflect a true “resting” baseline that is commonly collected in psychophysiological research (Quintana & Heathers, 2014). Acquiring resting baseline physiological data is a challenge across dyadic interaction studies that complicates the interpretation of HRV reactivity findings (Badovinac et al., 2023a). Due to this limitation, the finding of minimal changes between caregivers’ Baseline and Post 1 HRV may not be directly comparable to lab-based studies that include a resting baseline. Second, in line with the high educational attainment and low psychological distress symptomology of caregivers in our sample, generalizability to caregivers with sociodemographic risk related to low education or clinical levels of psychopathology may be limited, as these factors can impact both resting HRV and HRV reactivity to stressors (Laborde et al., 2017). Future work should characterize caregivers’ physiological responses to their child’s pain using a more socioeconomically diverse sample. Third, data on caregivers’ food intake, general physical activity levels, and medication use were not collected. These factors may have contributed to individual differences in caregivers’ baseline HRV levels (Quintana & Heathers, 2014). Fourth, because caregivers’ reports of their general parenting stress and anxiety symptoms were collected following the vaccination appointment, it is possible that events that occurred following the appointment may have influenced caregivers’ scores on these measures and attenuated their associations with caregiver HRV.

Conclusion

This study examined associations between caregivers’ physiological, psychological, and behavioral responses to toddlers’ pain-related distress. Using a universally standardized, naturalistic stressor, we described typical physiological responses, operationalized using a marker of parasympathetic nervous system activity, in a culturally diverse sample of caregivers. Results indicated minimal changes in caregivers’ parasympathetic activity levels from baseline to post-needle and slightly decreasing parasympathetic activity levels across the post-needle period. Caregivers with more parenting stress showed less vagal withdrawal across the post-needle period. This work contributes to an improved understanding of caregivers’ experiences of their toddlers’ pain and can inform future research focused on leveraging caregivers as the primary intervention for supporting children during painful experiences.

Footnotes

1

Based on the ethnocultural categories used by Statistics Canada (2021). Further detail is in Badovinac et al., (2023b).

Contributor Information

Shaylea D Badovinac, Department of Psychology, York University, Toronto, ON, Canada.

David B Flora, Department of Psychology, York University, Toronto, ON, Canada.

Heather Edgell, School of Kinesiology & Health Science, York University, Toronto, ON, Canada.

Dan Flanders, Department of Pediatrics, University of Toronto, Toronto, ON, Canada.

Hartley Garfield, Department of Pediatrics, University of Toronto, Toronto, ON, Canada; The Hospital for Sick Children, Toronto, ON, Canada.

Eitan Weinberg, Department of Pediatrics, University of Toronto, Toronto, ON, Canada.

Deena Savlov, Department of Pediatrics, University of Toronto, Toronto, ON, Canada.

Rebecca R Pillai Riddell, Department of Psychology, York University, Toronto, ON, Canada; Department of Pediatrics, University of Toronto, Toronto, ON, Canada; The Hospital for Sick Children, Toronto, ON, Canada.

Author contributions

Shaylea D. Badovinac (Conceptualization [lead], Formal analysis [lead], Methodology [lead], Project administration [lead], Writing—original draft [lead], Writing—review & editing [lead]), David Flora (Conceptualization [supporting], Formal analysis [supporting], Methodology [supporting], Writing—review & editing [supporting]), Heather Edgell (Conceptualization [supporting], Formal analysis [supporting], Methodology [supporting], Writing—review & editing [supporting]), Dan Flanders (Conceptualization [supporting], Methodology [supporting], Writing—review & editing [supporting]), Hartley Garfield (Conceptualization [supporting], Methodology [supporting], Writing—review & editing [supporting]), Eitan Weinberg (Conceptualization [supporting], Methodology [supporting], Writing—review & editing [supporting]), Deena Savlov (Conceptualization [supporting], Methodology [supporting], Writing—review & editing [supporting]), and Rebecca R. Pillai Riddell (Conceptualization [lead], Formal analysis [supporting], Methodology [lead], Project administration [lead], Supervision [lead], Writing—original draft [supporting], Writing—review & editing [lead])

Funding

This work was supported by the Natural Sciences and Engineering Research Council of Canada [# RGPIN-2020-07140, to RPR], Ontario Ministry of Research and Innovation [#532653, to RPR], Canadian Foundation for Innovation [#29908, to RPR], Canadian Institutes of Health Research [#GSD-164166, to SB], Ontario Graduate Scholarship [to SB], and Meighen Wright Graduate Scholarship in Maternal-Child Health [to SB]. Funders were not involved in study design or conduct.

Conflicts of interest: None declared.

Data availability

Data are available on request.

Research ethics

This study received ethical approval from the Institutional Review Board at York University (certificate # 2015-259).

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Data Availability Statement

Data are available on request.

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