Empathy in paediatric intensive care nurses part 2:

Neural correlates

Published in Journal of Advanced Nursing

Philip L. Jackson1,2,7, Margot Latimer3,4, Fanny Eugene1,2, Emily MacLeod3,

Tara Hatfield3, Etienne Vachon-Presseau5, Pierre-Emmanuel Michon1,2,

Kenneth M. Prkachin6

1 Centre interdisciplinaire de recherche en readaptation et integration sociale, Quebec, Quebec, Canada2 CERVO Research Center, Quebec City, Quebec, Canada3 IWK Health Centre, Halifax, Nova Scotia, Canada4 School of Nursing, Dalhousie University, Halifax, Nova Scotia, Canada5 Department of Physiology, Northwestern University, Evanston, IL, USA6 Department of Psychology, University of Northern British Columbia, Prince George, British Columbia, Canada7 School of Psychology, Universite Laval, Quebec, Quebec, Canada

Correspondence

Philip L. Jackson, Ecole de psychologieUniversite Laval, Quebec (Quebec) CanadaEmail: philip.jackson@psy.ulaval.ca

Funding information

This work was supported by an operating grant awarded to PLJ, ML, and KMP by the Canadian Institutes of Health Research grant #201203MOP-271954 and a salary award from the Fonds de Recherche du Quebec –Sante to PLJ

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ABSTRACT

Aims: To determine if there are brain activity differences between paediatric intensive care

nurses and allied health professionals during pain intensity rating tasks and test whether these

differences are related to the population observed (infant or adult) and professional experience.

Background: The underestimation of patients’ pain by healthcare professionals has generally

been associated with patterns of change in neural response to vicarious pain, notably reduced

activation in regions associated with affective sharing and increased activation in regions

associated with regulation, compared with controls. Paediatric nurses, however, have recently

been found to provide higher estimates of infants’ pain in comparison to allied health controls,

suggesting that changes in neural response of this population might be different than other

health professionals.

Design: Cross-sectional study.

Methods: Functional MRI data were acquired from September 2014–June 2015 and used to

compare changes in brain activity in 27 female paediatric care nurses and 24 allied health

professionals while rating the pain of infants and adults in a series of video clips.

Results: Paediatric nurses rated infant and adult pain higher than allied health professionals, but

the two groups’ neural response only differed during observation of infant pain; paediatric

nurses mainly showed significantly less activation in the medial prefrontal cortex (linked to

cognitive empathy) and in the left anterior insula and inferior frontal cortex (linked to affective

sharing).

Conclusions: Patterns of neural activity to vicarious pain may vary across healthcare professions

and patient populations and the amount of professional experience might explain part of these

differences.

KEYWORDS

Empathy, functional magnetic resonance imaging, infants, nurse-patient interaction, pain

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1. INTRODUCTION

The ability of caregivers to evaluate accurately their patients’ pain is crucial to proper

management. Unfortunately, multiple studies have shown that healthcare professionals tend to

underestimate patients’ pain (Prkachin, Solomon, & Ross, 2007) compared with the evaluations

of control participants without medical training (Cheng et al., 2007; Decety, Yang, & Cheng,

2010) and to the patients’ own evaluations (Coran, Koropeckyj-Cox, & Arnold, 2013; Efficace et

al., 2014; Kappesser, Williams, & Prkachin, 2006; Prkachin, Berzins, & Mercer, 1994; Puntillo,

Neighbor, O’Neil, & Nixon, 2003). While the cause of this pain underestimation remains unclear,

this phenomenon has been found to increase with caregiver’s experience (Choiniere, Melzack, &

Girard, 1990; Gleichgerrcht & Decety, 2014; Perry & Heidrich, 1982; Solomon, 2001) and has

been shown to be related to changes in the neural response to vicarious pain (Cheng et al.,

2007; Decety et al., 2010). Considering the prevalence of pain worldwide, gaining new

knowledge about the neural basis of response to patient pain exposure in healthcare

professionals could lead to objective markers of the tendency towards under management. The

relationship between under management and the different components of empathy, which

have been repeatedly shown to be involved in vicarious pain, could offer new insight into the

need for continuous training of nurses in pain management.

1.1 Background

Social neuroscience has examined the brain’s response to the pain of others mostly in

the context of empathy research, contributing to neurocognitive models of this complex and

multi-component process (e.g., Decety & Jackson, 2004; Zaki & Ochsner, 2012). These models

make a clear distinction between affective and cognitive components. Neural regions found to

be involved in the perception of self-pain and of others’ pain, such as the dorsal anterior

cingulate cortex (dACC) and anterior midcingulate cortex (aMCC) and a region including the

anterior insula (AI) and adjacent inferior frontal gyrus (IFG), are typically associated with

affective sharing of pain experiences (Lamm, Decety, & Singer, 2011; Shamay-Tsoory, Aharon-

Peretz, & Perry, 2009) and together form what is referred to as the salience network (Betti &

Aglioti, 2016). Other regions such as the temporoparietal junction (TPJ) and the medial

prefrontal cortex (mPFC) are thought to play a role in a component of empathy that involves

more controlled cognitive processes: mentalizing – i.e., the ability to perceive and understand

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others’ perspectives (Decety, Jackson, & Brunet, 2007; Frith & Frith, 2006; Saxe & Wexler, 2005;

Van Overwalle & Baetens, 2009; Zaki & Ochsner, 2012).

Expertise as a healthcare professional (i.e., degree of exposure to patient pain) seems to

modulate the neural responses to vicarious pain (Cheng et al., 2007; Decety et al., 2010).

Indeed, Cheng et al. (2007) showed that physicians with expertise in acupuncture, compared

with non-expert controls, showed less activation in the aMCC and the AI (regions associated

with affective sharing and saliency), during the observation of patients receiving painful needle

insertions. However, activation in the mPFC and the TPJ, regions associated with the cognitive

component of empathy, was stronger in physicians than in control participants. Expertise may

thus modulate neural mechanisms involved in healthcare professionals’ empathic response to

patients’ pain. More specifically, healthcare professionals may be less emotionally affected by

others’ pain and use more cognitive processes to evaluate this pain than non-healthcare

professionals. As the mPFC is shown to be involved in regulation processes in emotion research

(Etkin, B€uchel, & Gross, 2015; Ochsner & Gross, 2008), its higher activation in healthcare

professionals could also reflect the action of regulatory (self-protective) processes inhibiting the

affective response to vicarious pain (Cheng et al., 2007). Thus, regulation in the context of the

neural basis of empathy, is more a reflection of the weight given to the two distinct components

of empathy (affective [affective sharing] and cognitive [mentalizing]) rather than a discrete and

neuro-functionally independent component. This is also consistent with the concept of detached

concern that allows healthcare professionals to care for their patients without becoming

emotionally overinvolved (Lief & Fox, 1963; Newton, 2013). Of relevance, Cheng et al. (2007)

also reported that stronger activation in aMCC and AI (affective network) during the observation

of others’ pain was associated with higher pain estimates, while stronger activation in mPFC

(mentalizing network) was associated with lower estimates. This pattern could thus partly

explain healthcare professionals’ underestimation of patients’ pain.

Although pre-existing (predisposing) characteristics of individuals who choose to pursue

careers as healthcare professionals cannot be ruled out, differences observed between

paediatric experts’ and non-experts’ neural response likely results in part from their experience

as a healthcare professional. Indeed, a recent study has shown that exposure to vicarious pain

can modulate the subsequent neural response to other’s pain, for instance dampening

activation in the AI (Preis, Kröner-Herwig, Schmidt-Samoa, Dechent, & Barke, 2015).

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Furthermore, experience as a healthcare professional has been associated with a decrease in

estimates of patients’ pain intensity (Gleichgerrcht & Decety, 2014) and more generally, a

decline in empathy has been observed during medical training (Hojat et al., 2009; Newton,

Barber, Clardy, Cleveland, & O’Sullivan, 2008).

These different findings have mostly been demonstrated in the context of adult pain.

Such findings may not generalize to paediatric pain as pain assessment in young children,

especially infants, relies on cues that may differ from those used to evaluate adult pain.

In one study that specifically examined the association between expertise and pain

appraisal in infants, paediatric nurses were found to provide higher pain estimates compared

with allied health professionals (Latimer, Jackson, Johnston, & Vine, 2011). This finding,

contradictory with what is typically found in the adult literature, suggests that clinical training

and expertise with pain in infants could increase, rather than decrease, paediatric nurses’

sensitivity to this pain. Therefore, the expected increased rating of pain in paediatric nurses

could be accompanied by greater involvement of neural regions associated with affective

sharing and/or reduced involvement of neural regions associated with cognitive empathy

processes in response to infant patients’ pain.

The present paper is Part 2 of a set of papers reporting the results of a study of empathy

for pain in paediatric nurses. Knowing that paediatric nurses rated infant and adult pain

significantly higher than a comparison group of allied health professionals (AHPs; Part 1, Latimer

et al., 2017), this paper focuses on the neuroimaging results; comparing the brain response

during pain assessment in these same participants.

2. THE STUDY

2.1 Aims

The first aim of this study was to compare paediatric nurses’ (i.e., nurses working in the

neonatal and paediatric intensive care units of a paediatric hospital) behavioural (i.e., pain

rating) and neural responses to infant pain to those of AHPs. A second aim of this study was to

examine whether paediatric nurses’ behavioural and neural responses to vicarious pain were

associated with years of professional experience. A final aim of this study was to examine the

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specificity of expertise-related differences found in paediatric nurses, exposed daily to infant

and child pain, by also examining their behavioural and neural responses to adult pain.

2.2 Design

2.2.1 Participants

Twenty-seven female nurses working in the neonatal and paediatric intensive care units

(NICU, PICU) of a Canadian children’s hospital were recruited. Twenty-six age- and experience-

matched AHPs (e.g., pharmacists, social workers) not regularly exposed to patients’ pain were

recruited from the same hospital to serve as a control group. Note that two participants from

the control group had to be excluded on the basis of excessive movement during the fMRI

acquisition, leaving 24 participants in the control group. All participants had to be right-handed

and have no history of psychiatric, neurological, or pain-related disorders (Table 1). Typical

restrictions based on magnetic resonance imaging (MRI) compatibility were also used as

exclusion criteria (e.g., claustrophobia, metal implants).

TABLE 1 Demographic data for each group of participants that completed the study and for which the data were included in the analyses

Nurse group Control group

Number of participants [NICU] [PICU] 27 [24] [3] 24

Age (SD) 36.4 (10.6) 36.8 (7.1)

Number of years of experience (SD) 11.5 (10.1) 7.8 (6.5)

Note that the breakdown for nurses recruited from the Neonatal Intensive Care Unit (NICU) and Paediatric Intensive Care Unit PICU) is provided in brackets; Age and Number of years of experience are reported in years; standard deviations (SDs) are shown in parenthesis. Note that one participant in each group did not complete the Adult Pain Task, yielding totals of n = 26 and n = 23, for the Nurse and Control groups, respectively, for these results specifically.

2.3 Data Collection

2.3.1 Stimuli

Stimuli used in the Infant Pain task were 18, seven-second ecological videos of neonates

(35–41 weeks’ gestation) undergoing painful and non-painful procedures in the NICU. All videos

were taken from the validated Empathy for Infant Pain video program and presented infants

showing no pain (n = 6), low pain (n = 6), or high pain (n = 6) levels (see Latimer et al., 2011 for a

detailed description of validation procedures). Stimuli used in the Adult Pain task were 18,

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seven-second videos of adult shoulder pain patients undergoing range of motion tests. All

videos were taken from the UNBC-McMaster Shoulder Pain database (Prkachin & Solomon,

2008) and showed adult male and female faces (framed from the neck up) expressing no pain (n

= 6), low pain (n = 6), or high pain (n = 6) levels.

2.3.2 Pain evaluation tasks

The Infant Pain and Adult Pain tasks were identical except for the video stimuli used

(infant or adult). Trials for both tasks consisted of a seven-second video, followed by a visual

analogue scale (VAS) ranging from “No pain” - “Highest Pain”. Participants were asked to rate

the intensity of pain displayed by the person in the video, by using two buttons on a response

box to move the cursor from left to right with the index and middle finger of their right hand.

The initial position of the cursor was determined randomly for each trial. The VAS remained on

the screen for 7 s followed by a fixation cross of varying duration (jittered between 2-8 s; mean =

3.4 s), which was followed by the next trial. Each run included 18 trials (six per pain level

presented pseudo-randomly; i.e., no more than two consecutive trials with the same pain level).

Three runs were completed with the Infant Pain task followed by three runs with the Adult Pain.

Participants performed three practice trials in the scanner (using other similar videos) before the

first scan.

2.3.3 Procedures

Participants were recruited through posters around the hospital and advertisements on

the hospital’s intranet, as well as through word of mouth between employees. Prior to their MRI

participants completed their informed consent process (including signed consent form), MRI

screening and a demographic questionnaire.

Participants who met MRI safety criteria were contacted shortly after this initial meeting

to schedule their MRI session. Time between these two sessions varied depending on the

participants’ availabilities, but the median delay was 18 days. Consent and MRI screening forms

were reviewed with participants on arrival for the MRI session. This session included functional

MRI acquisition during which participants performed the Infant Pain and the Adult Pain tasks,

followed by a structural scan. To help reduce motion during scanning, padding was used inside

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the head coil. Functional magnetic resonance imaging data were acquired between September

2014 and June 2015.

fMRI acquisition parameters

Participants were scanned in a 4T Agilent/OMT whole body scanner. Functional images

were acquired using a T2*-weighted two-shot spiralout descending sequence with the following

parameters: TR = 2000 ms, TE = 15 ms, flip angle = 60°, FOV= 240 9 240 mm, in-plane matrix = 64

9 64, 30 slices (3.5 mm thick with a 0.5 mm gap, yielding a voxel size of 3.75 9 3.75 9 3.5 mm). A

structural scan was acquired for each participant after the functional scans using a T1-weighted

3D IR-prepped FLASH sequence with the following parameters: TI = 500 ms; TR/TE = 10/5 ms;

flip angle = 11°; FOV= 240 9 240 mm; matrix = 256 9 256 voxel; 170 slices; slice = 1.0 mm.

2.4 Ethical considerations

This study was approved by the Internal Review Boards of the Institut de readaptation

en deficience physique de Quebec and the IWK Health Centre. Participants received a monetary

compensation of $75 for their participation.

2.5 Validity and reliability

The visual stimuli used in this fMRI study for both Infant and Adult Pain tasks have been

validated and used in several previous behavioural (Infant: Latimer et al., 2011; Adult: Prkachin

& Solomon, 2008) and fMRI studies (Botvinick et al., 2005). To our knowledge this study is the

first fMRI study to use the Infant Pain task, but the validation procedure, which considered

stimulus quality, duration and content validity, was conducted with the anticipated objective of

using it in an fMRI experiment. Similar fMRI procedures with visual stimuli depicting pain have

been repeatedly used by PLJ, his team and colleagues (e.g., Jackson, Meltzoff, & Decety, 2005,

Jackson, Meltzoff, & Decety, 2006, Vachon-Presseau et al., 2012).

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2.6 Data analysis

2.6.1 Behavioural data analysis

Note that pain ratings reported here are also presented in Part 1 of this project (see

Latimer et al., 2017), which examines a series of psychosocial measures taken from the same

samples enrolled in a larger scale study. Behavioural and imaging data were analyzed separately

for each task because the Infant Pain and Adult Pain tasks were quite different in terms of

stimuli shown and because the tasks were always performed in the same order (see

Limitations). Behavioural data from each task were analysed using SPSS 22. For pain intensity

ratings, trials on which participants did not respond or on which they were still moving the

cursor when the VAS disappeared from the screen (i.e., errors), were excluded from behavioural

analyses (Infant Pain and Adult Pain tasks, respectively: 13% and 13% in controls, 17% and 15%

in nurses; t < 1 (n.s.) in each task). In both groups, the assumption of normal distribution for pain

intensity ratings was violated for each task (based on Shapiro–Wilk tests) so generalized

estimating equations based on a gamma distribution model were used to calculate main effects

and interactions. Post hoc comparisons were performed using Mann–Whitney U tests for

independent samples with a Bonferroni correction to identify between group differences in

ratings at each level of pain.

2.6.2 Imaging data pre-processing and analysis

All functional scans were first despiked using AFNI’s 3dDespike (Cox, 1996) and then pre-

processed and analysed using SPM8 software (Wellcome Department of Imaging Neuroscience,

London, UK). For each participant, functional images were first realigned to correct for head

motion, co-registered to the anatomical images, normalised into the Montreal Neurological

Institute standard stereotaxic space with voxels resampled to 3 9 3 9 3 mm and spatially

smoothed using a three-dimensional Gaussian kernel of 8 mm full-width at half-maximum.

Artifact Detection Tools (ART; http://www.nitrc.org/projects/artifact_detect/) software was

used to ensure that no dataset contained scan-to-scan movement exceeding 3 mm (combined

rotation and translation) and to identify potential abnormalities in global mean signal intensity.

Volumes with an important drop in global signal intensity (>5 SD below the session mean) were

identified for one nurse (2% of volumes) and one control participant (4% of volumes) during the

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Infant Pain task; these outlier volumes were excluded from first-level analyses by including an

additional regressor for each.

Contrast analyses

Analyses were performed separately for each pain evaluation task. For each participant,

a first-level general linear model was specified with two regressors for each level of pain (video

and response period) and six regressors to account for residual motion. For each task, contrasts

were performed between activation during observation of pain and no pain stimuli. Results from

those first-level comparisons were then used as input in one-sample t-tests for each group and a

between group two-sample t-test. AFNI’s 3dFWHMx was used to determine smoothness of data

(xyz = 13 12 12), which was used in AFNI’s 3dClustSim, yielding a cluster size-corrected alpha

of .05 combining a cluster size threshold of k ≥ 39 at a voxel-wise threshold of p < .001.

2.6.3 Correlational analyses

Region of interests (ROI) masks were created using Marsbar (Brett, Anton, Valabregue,

& Poline, 2002) by tracing 10 mm radius spheres around the maximum peak for each significant

cluster in the two-sample t-test results. For each task and for each participant, parameter

estimates in the contrast pain (low pain + high pain) > no pain were extracted from these ROIs.

Correlational analyses were performed to determine whether neural activation in each region

was correlated with experience and/or with intensity ratings provided for the pain stimuli. As

data from three different ROIs were tested in these analyses, Bonferroni corrected thresholds

were used (alpha = .05/3 = .017). Bivariate correlational analyses were also performed to

examine the relationship between pain intensity ratings and years of experience.

3 RESULTS

3.1 Demographic and experience data

Non-parametric tests were used to ensure that groups were comparable in age and

experience, as Shapiro–Wilk tests indicated that these two variables were not normally

distributed in each group. A Mann–Whitney test showed that there was no significant difference

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between the two groups on either age (Mann–Whitney U = 294, p = .571) or number of years of

experience (Mann–Whitney U = 265, p = .265) in their current position. Two of the participants

(one per group) were unable to complete the Adult Pain task, leaving group sizes of 26 nurses

and 23 control participants for the Adult Pain results. These reduced groups were not

significantly different in terms of age (Mann–Whitney U = 260.5, p = .440) or years of experience

(Mann–Whitney U = 251.5, p = .340).

3.2 Pain intensity ratings

3.2.1 Infant pain task

Generalized estimating equations on pain intensity ratings revealed significant main

effects of pain level (Wald Chi-Square = 348.85, p < .001) and group (Wald Chi-Square = 5.78, p =

.016) and a significant pain by group interaction (Wald Chi-Square = 9.98, p = .007). Post hoc

Mann–Whitney tests (Bonferroni corrected alpha of 0.05/3 = .0167) revealed that ratings for the

non-painful stimuli were not statistically different between nurses and control group

participants (U = 269.0, p = .299), but nurses gave significantly higher pain ratings than control

participants for low pain (U = 133.5, p < .001) and high pain (U = 166.5, p = .003) stimuli (see

Figure 1a).

3.2.2 Adult pain task

Generalized estimating equations on pain intensity ratings revealed significant main

effects of pain level (Wald Chi-Square = 416.22, p < .001) and group (Wald Chi-Square = 6.8, p

= .009) and a significant pain by group interaction (Wald Chi-Square = 9.76, p = .008). Post hoc

Mann–Whitney tests (Bonferroni corrected alpha of 0.05/3 = .0167) revealed that ratings for the

non-painful stimuli were not statistically different between nurses and control group

participants (U = 207.0, p = .065), but nurses gave significantly higher pain ratings than control

participants for the low pain (U = 171.0, p = .010) stimuli. Nurses’ ratings for the high pain

stimuli were also higher than controls’ but this difference was only significant at an uncorrected

alpha threshold (U = 199.0, p = .045) (Figure 1b).

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F IGURE 1 Mean pain intensity ratings for each group in the Infant Pain task (a) and the Adult Pain task (b). Error bars represent one standard error. *p < .05; **p < .005; ***p < .001

3.3 Imaging data results

3.3.1 Infant pain task

In the control group, observation of pain (compared with no pain) in infants was

associated with significant activation in a cluster extending from the aMCC to the supplementary

motor area (SMA), a cluster extending from the left pars opercularis of the inferior frontal gyrus

(IFG) to the adjacent anterior insula (AI) and clusters in the periaqueductal gray (PAG), the

posterior part of the superior temporal sulcus (pSTS) and the left dorsal premotor cortex. In

nurses, the same contrast yielded no significant activation. The direct between group

comparison showed that in paediatric nurses, observation of pain, compared with no pain, in

infants was associated with significantly less activation in the left IFG/AI, the mPFC and the right

thalamus, than in controls (Figure 2a). No region was significantly more activated in nurses than

in controls for this contrast (Table 2).

3.3.2 Adult pain task

In the control group, observation of pain (compared with no pain) in adults was

associated with significant activation in the right pSTS, the SMA and the visual cortex (mostly

V1). In nurses, the same contrast yielded significant activation in the right pSTS and the

SMA/aMCC. The direct between-group comparison yielded no significant difference between

paediatric nurses’ and AHPs’ neural response to adult pain (Table 3).

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3.3.3 Correlational analyses

A significant negative correlation was found between IFG/AI activation in response to

infant pain (compared with no pain) and number of years of experience (r(49) = .377, p = .006).

When groups wereexamined separately, this correlation was observed in nurses (r (25) = .480, p

= .011; Figure 2b) but not in the control group. When the two groups were pooled together,

there was also a significant negative correlation between ratings and thalamus activation (r

= .340, p = .015). However, correlations between pain intensity ratings and neural activation in

ROIs failed to reach significance when each group was examined separately. There were no

significant correlations between experience and pain intensity ratings in either task, in either

group.

F IGURE 2 (a) Areas in which paediatric nurses showed significantly less activation (p < .001, k ≥ 39) than non-expert controls during the observation of infant pain (vs. no pain) stimuli. AI = anterior insula; IFG = inferior frontal gyrus; L = left; mPFC = medial prefrontal cortex; R = right. (b) Correlation between years of experience and parameter estimates extracted from a 10 mm radius sphere around peak of IFG/AI cluster. [Colour figure can be viewed at wileyonline library.com]

TABLE 2 Infant pain taskPeak conditionX Y Z K Z

Control groupAnterior mid cingulate cortex/Supplementary motor area 6 8 61 109 4.06Inferior frontal gyrus/Anterior insula -48 8 13 72 4.87Precentral gyrus -30 -1 58 143 3.80Periaqueductal gray -6 -31 -2 48 4.21Posterior superior temporal sulcus 48 -37 4 72 4.17

Nurse group: No suprathreshold clusterControl > NurseMedial prefrontal cortex 12 41 46 40 3.53Inferior frontal gyrus/Anterior insula -33 23 -14 40 3.58Thalamus 9 -10 7 58 3.66

Nurse > Control: No suprathreshold cluster

Cerebral regions ordered from the most anterior to the most posterior showing significant activation in the Pain > No Pain contrasts during the Infant Pain task, within each group (Control group and Nurse group), and in the between-group contrasts (Control>Nurse

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and Nurse>Control), at a cluster-corrected family wise alpha of .05 (uncorrected p < .001 and k ≥ 39). Peak locations are reported using x, y, and z standard coordinates from Montreal Neurological Institute (MNI) space; k = number of voxels found for each significant cluster; Z = Z statistic value.

4. DISCUSSION

Our program of research is the first to compare neural responses of healthcare

professionals to those of allied healthcare professionals less exposed to vicarious pain, during

the assessment of pain in distinct populations of patients.

4.1 Behavioural and neural differences between paediatric nurses and allied health

professional controls (Aim 1)

Results from the Infant Pain task replicated previous findings (Latimer et al., 2011),

confirming that paediatric nurses’ estimates of observed infant pain intensity were higher than

those of control group participants. This finding seems even more robust for low intensity pain

stimuli, which could underline the fact that expertise effects are more discernible when fewer

cues are available to assess pain.

The idea of a self-protective reduction of vicarious pain responses in healthcare

professionals has been suggested as an explanation for previous neuroimaging results showing

that compared with controls, physicians’ neural response to adult patients’ pain was

characterized by reduced activation in regions associated with affective sharing (aMCC and AI)

and increased activation in the mPFC, involved in the cognitive component of empathy (Cheng

et al., 2007). Based on previous findings (Latimer et al., 2011), it was expected that nurses would

show an opposite pattern in their neural response to infant pain compared with controls; more

activation in regions associated with affective sharing and less activation in regions associated

with the cognitive component of empathy. This was only partially confirmed. As hypothesized,

paediatric nurses responded to infant pain with less activation than controls in the mPFC and

higher pain ratings. In another study, the opposite pattern was found in physicians (i.e.,

increased mPFC activity and underestimation of patients’ pain), which had been interpreted as

potentially resulting from a self-protective bias that would dampen physicians’ vicarious

response to pain and keep them from sharing too much of their patients’ distress (see also

Newton, 2013). The results of the current study showing higher pain ratings and relatively lower

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mPFC response to infant pain in paediatric nurses suggest that this group of healthcare

professionals may lack this self-protective bias and show less regulation in the context of

vicarious pain. However, given that we did not measure self-regulation directly additional

research is needed to draw specific conclusions regarding the link between these results and a

potential self-protective bias.

Moreover, paediatric nurses in the present study responded to infants’ pain with less

activation than controls in the IFG/AI and the thalamus, regions associated with affective sharing

of others’ pain (Lamm et al., 2011) which goes against the hypothesis that their higher

assessment of infant pain results from increased affective sharing processes. In fact, differences

observed here between nurses’ and controls’ neural responses to infant pain were not

associated with differences in pain intensity ratings (as in Cheng et al., 2007).

4.2 Nurses’ response to infant pain in IFG/AI decreases with experience (Aim 2)

Previous results showing reduced activation in regions associated with affective sharing

in healthcare professionals have been linked to expertise (Cheng et al., 2007), but an alternative

explanation could be that this dampened response reflects pre-existing differences that could

predispose some individuals to pursue healthcare professions. However, the current study

showed that IFG/AI response to infant pain was lower in more experienced than less

experienced nurses, which supports the formulation that reduced activation in this region is

related, at least partly, to their work as paediatric nurses. This adds to the evidence that

paediatric nurses’ chronic exposure to infant pain leads to a habituation effect in the IFG/AI

response to this pain. Of relevance, a previous study (Tei et al., 2014) has shown that activation

in this region in response to vicarious pain was lower in nurses with higher symptoms of

burnout.

4.3 The relative specificity of the paediatric nurses’ behavioural and neural responses (Aim 3)

The current study expanded on our previous results (Latimer et al., 2011) by showing

that paediatric nurses also provided higher estimates of perceived pain intensity than controls in

the Adult Pain task. By showing that paediatric nurses’ higher estimation of patients’ pain is not

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specific to the population with which they have the most expertise, these findings could suggest

that paediatric nurses are more sensitive to vicarious pain in general.

Despite nurses rating adult patients’ pain higher than AHP controls, the two groups’

neural response to these stimuli did not differ significantly. Both groups had significant

activation in the aMCC, associated with affective sharing of vicarious pain (Lamm et al., 2011)

and in the right pSTS, associated with cognitive processes involved in empathy (e.g., mentalizing;

Frith & Frith, 2006; Zaki & Ochsner, 2012) and specifically with the perception of pain facial

expressions (Vachon-Presseau et al., 2012). Although paediatric nurses’ ratings were higher on

both tasks, their neural response to patients’ pain only differed from that of controls for the

infant pain. This suggests that the link between expertise and neural response to vicarious pain

may be more specific to the care population than its link to pain assessment. Together, these

findings are compatible with the interpretation that healthcare professionals show expertise-

related changes in their neural response to patients’ pain and that this effect is specific to the

type of pain they most frequently encounter in their practice.

Such habituation may be due to repeated exposure. As nearly all nurses in this study

worked in the neonatal intensive care unit (NICU) and the others worked in the paediatric ICU,

they were all exposed frequently to infant pain. More importantly, infant pain videos were

filmed in the NICU and showed procedures that these nurses routinely perform every day.

Repeated exposure to a specific type of pain could lead to a blunting of the neural response to

this pain, as suggested by a recent study (Preis et al., 2015) showing that repeated exposure to

stimuli showing hands in painful contexts was associated with a reduced neural response to

these stimuli (without changes in pain ratings as well). As one of the regions where this blunting

was observed was the AI, this suggests that a similar neural habituation following repeated

exposure to patients in pain could explain the nurses’ reduced IFG/AI activation to infant pain.

4.4 What is different about paediatric nurses?

Results showing that paediatric nurses provided higher estimates of both infant and

adult pain than AHP controls suggest a generalized effect in paediatric intensive care nurses. It

should be noted that nurses’ pain intensity ratings here were compared only to those of AHP

controls and not to the patients’ own evaluation of their pain and it is thus impossible to

determine whether they actually overestimated this pain. Also, while literature reviews reveal a

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general tendency for underestimation (Prkachin et al., 2007; Solomon, 2001), there have been a

few reports of overestimation by non-paediatric healthcare professionals, when patients

reported low pain intensity levels (Olden, Jordan, Sakima, & Grass, 1995; Zalon, 1993) or no pain

(Heikkinen, Salanter€a, Kettu, & Taittonen, 2005). Here, however, both low pain and high pain

stimuli elicited higher pain intensity ratings from nurses than from controls.

Another explanation for the higher pain ratings in paediatric nurses than controls may

reside in the type of relationships these professionals develop with their patients, as aspects of

patient-caregiver relationships influence pain assessment (Coll, Gregoire, Latimer, Eugene, &

Jackson, 2011). For instance, closer patient–caregiver relationships may be associated with

higher estimates of patient pain, as indicated by reports of overestimation of patients’ pain by

family caregivers (Redinbaugh, Baum, DeMoss, Fello, & Arnold, 2002; Yeager, Miaskowski,

Dibble, & Wallhagen, 1995). Paediatric nurses may become more involved with their patients

than healthcare professionals who work mostly with adult patients. This last point, together

with the findings of Tei et al. (2014) who showed more burnout in nurses, raises an important

issue that needs to be taken into consideration in the training of nurses working in ICUs. Sharing

pain vicariously and repetitively does come with some cost and while experience may attenuate

part of the affective response, such change might occur at the expense of nurses’ mental health.

Even though more studies are necessary to document the link between neural responses and

actual care the current findings suggest that nurses should be informed during training about

potential changes in brain function found after repetitive exposure to pain and perhaps even

other forms of suffering as well (Zaki, Wager, Singer, Keysers, & Gazzola, 2016).

4.5 Limitations

Both NICU and PICU nurses were eligible to participate in the study but the majority of

the participants in the Nurse Group were from the NICU (24 of 27), thereby reducing the

potential generalization of the findings to PICU nurses. Another limitation concerns the

generalizability of the findings from a controlled MRI setting to the clinic. The behavioural

findings are consistent with those of a previous study (Latimer et al., 2011) conducted on

another sample outside the scanner but, whether pain ratings are indicative of pain

management strategies adopted remains to be tested. Finally, as the main focus of the study

was infant pain, we chose not to randomize the pain tasks and presented the infant pain task

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first. This could have introduced some bias in the adult pain task (carry-over effect, fatigue) and

replication of this task with a similar group of healthcare professionals but using a randomized

design is warranted.

5. CONCLUSION

This study shows that the relationship between expertise, neural response, and

evaluation of vicarious pain is more complex than suggested by the adult pain literature and

may vary across healthcare professions and patient populations. This emphasizes the

importance of conducting research specifically examining processes involved in the assessment

of infant pain, especially given that this population is entirely dependent on caregivers’

assessment of their pain, as they cannot communicate it verbally. Untreated pain can have

detrimental short and long-term impacts on a child but may also alter the cognitive and brain

functional architecture of their caregivers. Continued research on these processes involved in

pain management decisions is crucial considering the high rate of unmanaged pain in

hospitalized infants despite paediatric nurses’ knowledge of proper pain management and their

demonstrated ability to evaluate this pain (Cruz, Fernandes, & Oliveira, 2016; Latimer, Johnston,

Ritchie, Clarke, & Gilin, 2009).

ACKNOWLEDGEMENTS

The authors thank David McAllindon for his skillful technical assistance with fMRI data

acquisition and Sarah-Maude Deschenes for coordinating several aspects of the study.

CONFLICT OF INTEREST

No conflict of interest has been declared by the authors.

AUTHOR CONTRIBUTIONS

All authors have agreed on the final version and meet at least one of the following criteria

[recommended by the ICMJE (http://www.icmje.org/recommendations/)]:

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Substantial contributions to conception and design, acquisition of data, or analysis and

interpretation of data;

Drafting the article or revising it critically for important intellectual content.

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