Biobehavioral Measures for Pain in the Pediatric Patient

Review Article

From the Virginia Commonwealth

University School of Nursing,

Richmond, Virginia.

Address correspondence to

Mamoona Arif-Rahu, RN, PhD,

CCRN, VCU Medical Center, 1250 E.

Marshall Street, Box 985825,

Richmond, VA 23298. E-mail:

[email protected]

Received November 30, 2009;

Revised October 26, 2010;

Accepted October 26, 2010.

1524-9042/$36.00

� 2012 by the American Society for

Pain Management Nursing

doi:10.1016/j.pmn.2010.10.036

Biobehavioral Measuresfor Pain in the PediatricPatient

--- Mamoona Arif-Rahu, RN, PhD, CCRN,

Deborah Fisher, RN, MS, CS, CPON,

and Yui Matsuda, RN, BSN

- ABSTRACT:Pain is a complex biobehavioral phenomenon. The quantification of

pain involves the incorporation of many factors, including physio-

logic, behavioral, and psychologic factors. Recognition of pain relies

heavily on the expression of the patient as well as the interpretation of

the caregiver. There aremany studies published on biobehavioral pain

assessment tools, such as neuroimaging, neuromuscular, biomarker,

and behavioral pain assessment scales. These tools present a clinical

challenge to appropriately assess and manage pain in the noncom-

municative pediatric patients, such as infants, preverbal toddlers, and

intubated and/or unconscious or cognitively impaired patients. Pain is

a combination of physiologic, behavioral, and psychologic interac-

tions. Any tool that incorporates themeasurement of only one of those

domains is inherently incomplete in the assessment of pain. There-

fore, the purpose of this literature review was to provide a compre-

hensive overview of these biobehavioral pain assessment tools used in

pain assessment in the noncommunicative pediatric population.

� 2012 by the American Society for Pain Management Nursing

Pain is a complex biobehavioral phenomenon still not fully understood by re-

searchers and clinicians alike. The goal of objectifying a highly subjective phe-nomenon in a noncommunicative pediatric population continues to perplex

many researchers. For the nonverbal population, the American Society for Pain

Management Nursing (ASPMN) recommends using multidimensional instru-

ments that are characterized by both behavioral and physiologic indicators of

pain (Herr, Coyne, Key, Manworren, McCaffery, Merkel, Pelosi-Kelly, & Wild,

2006). There are several studies that have addressed the need for a pain assess-

ment tool that uses multimodal variables (Buttner & Finke, 2000; Gregg, 1998;

Labus, Keefe, & Jensen, 2003; Ramelet, Abu-Saad, Rees, & McDonald, 2004).The three approaches to pain assessment include cognitive (self-report),

behavioral (cry, posture, and facial expression), and physiologic (heart rate

variability, blood pressure fluctuations, decreases in oxygen saturation, and

metabolic and endocrine increases). Of all of these options, self-report is still

the gold standard in pain assessment. Unfortunately, when children cannot ex-

press themselves, self-report is not possible; further investigations and observa-

tions are needed for accurate pain assessment. Over the past 2 decades, there

have been an increasing number of studies published on biobehavioral

Pain Management Nursing, Vol 13, No 3 (September), 2012: pp 157-168

mailto:[email protected]

http://dx.doi.org/10.1016/j.pmn.2010.10.036

158 Arif-Rahu, Fisher, and Matsuda

assessment tools such as neuroimaging, neuromuscu-

lar, biomarker, and behavioral pain assessment scales.

ASSESSING PAIN IN PEDIATRICPATIENTS

Neuromuscular Activity of PainThe quantification of pain involves the incorporation

of many imprecise factors, so measurements tend tobe very subjective, relying heavily on the expression

of the patient as well as the interpretation of the care-

giver. An objective pain measurement tool would pro-

vide those in the clinical arena with a standardized

form of measurement that would not vary with patient

or caregiver. With this as a goal, various researchers

have evaluated the use of electroencephalography

(EEG), electromyography (EMG), and brain imagingtechniques as the basis for such objective measure-

ments of pain (Davis, Taylor, Crawley, Wood, &

Mikulis, 1997; Dowman, Rissacher, & Schuckers, 2008;

Henderson, Gandevia, & Macefield, 2008; Jancke,

Vogt, Musial, Lutz, & Theodor, 1996; Raux, Ray, Prella,

Duguet, Demoule, & Similowski, 2007).

EEG is readily available in thehospital setting for use

on a wide range of patients, which makes it a tool of in-terest in research applications. It provides a noninvasive

measurement of cortical brain activity. This activity can

be measured by application of electrodes to the scalp

and measurements taken at various band frequencies.

It has been shown that the somatosensory cortex, the an-

terior cingulate cortex, and the somatosensory associa-

tion areas located in the parietal operculum and insula

are activated by painful stimuli (Apkarian, Bushnell,Treede,&Zubieta, 2005). Dowman et al., (2008) studied

the pain-related cortical activity of the brain by using

EEG during tonic experimental pain stimulus and con-

trol conditions. They observed pain-related changes in

the EEG at specific electrode locations, such as the con-

tralateral central, frontocentral, and temporal scalp re-

gions. Their results indicated that pain-related changes

in the EEG showed a decrease in alpha over the contra-lateral temporal scalp (Newman–Keuls test: p < .05).

Raux et al., (2007) used EEG to demonstrate a pre-

motor cortical activation during a situation mimicking

one form of patient-ventilator asynchrony in noninva-

sive ventilated patients. The basis of the Raux et al.,

(2007) study was the underlying association between

specific brain regions and the control of breathing by

use of EEG. The results indicated that mean inspiratoryflow increased during ‘‘discomfort’’ compared with

the two ‘‘comfort’’ periods (p ¼ .0003). Furthermore,

the EEG results indicated that motor potentials were

significantly more frequent during ‘‘discomfort’’ than

during any of the ‘‘comfort’’ conditions (Fisher exact

test: p < .001) and thus are associated with an activa-

tion of the premotor cerebral cortex. Although EEG

may be a valid tool to measure brain activities associ-

ated with pain response, it requires trained technician

time to apply electrodes and translate results, therefore

making it impractical for clinical settings.

EMG has been widely used in the assessment ofpain in various regions of the body. EMG registers mus-

cle activity with surface electrodes. Several studies

have used EMG to study facial expressions by using in-

tensity of muscular response in patients suffering from

back pain, headache, and neck and shoulder pain

(Cram & Steger, 1983; Ong, Nicholoson, & Gramling,

2003; Sonnby-Borgstrom, 2002; Weyers, Muhlberger,

Hefele, & Pauli, 2006; Wolf, Raedler, Henke, Kiefer,Mass, Quante, & Wiedemann, 2005). Wolf et al.,

(2005) validated a facial EMG method for the measure-

ment of facial pain expression in ten healthy subjects

induced with a laser system pain stimulus. They stud-

ied nine muscle groups of the face. The results indi-

cated two groups of muscles corresponding to pain

expression. The first muscle group identified is assem-

bled around the orbicularis oculi muscle, which initi-ates staring. The second group consists of the

mentalis and depressor anguli oris muscles, both of

which trigger mouth movements. The investigators

recommended further studies with psychometric mea-

surements, a larger sample size, and a female test

group. Another study, by Jancke et al. (1996), exam-

ined the changes in facial EMG to auditory stimuli.

They found that when high-intensity stimuli were ad-ministered to subjects, a strong upper-face EMG re-

cording was observed. Similarly, in response to the

crying of a baby, muscle activity in the mouth region

increased.

So although EMG can be used to measure facial

muscular activity, which can be used as an indicator

of pain, EMG on its own should not be used as a direct

absolute measurement of pain, in either a research set-ting or a clinical setting. One of the main drawbacks in

the use of objective measurements such as EEG, EMG,

and other brain imaging techniques is that there is

a lack of research on the associated interpretation of

the emotional response of patients (Jancke et al.,

1996). In addition, intersubject reliability can be influ-

enced by lead placement, possibly leading to inconsis-

tent results.Although a myriad of brain imaging techniques ex-

ist, the main one used in the assessment of pain is mag-

netic resonance imaging (MRI). This is largely due to

the fact that MRI is noninvasive and has a combination

of high temporal and spatial resolution. A study done

by Henderson et al., (2008) demonstrated gender differ-

ences in functional MRI measurements made during

TABLE 1.

Chemical Biomarkers for Pain

Biomarker (receptor) Pathophysiologic Role Pharmacologic Modulation

b-Endorphin Produced by fetal pituitary gland.c

An opioid peptide produced by leukocytes and released inresponse to pain and/or stress; antinociceptive effect.cde

Opioidse

Interleukin (IL) 1b Proinflammatory cytokine.f

Stimulates secretion of opioid peptides from leukocytes.b

IL-4 Antiinflammatory cytokine produced by lymphocytes and mastcells.fg

Analgesic effect by inhibition of TNF-a, IL-8, and IL-1b.f

IL-8 (CXCR1) Proinflammatory cytokine involved in inflammatory,hypernociception and neuropathic pain; induces mechanicalhypernociception.f

Produced by macrophages.g

b-Adrenergic receptorantagonistsf

Metenkephalin Opioid peptide with antinociceptive effect as analgesicmediator.bd

Opioidsd

Serotonin (5HT) Acts as a stimulant for nociceptive nerve endings; found inplatelets and basophils.a

5-HT3 antagonistsa

Tumor necrosis factor(TNF) a (TNFR1)

Proinflammatory cytokine produced by macrophages; directsensitization of nociceptors.f

Present in neurons and glia; involved in inflammatory andneuropathic hyperalgesia.g

Indomethacin, infliximab,etanercept, adalimumab,thalidomide, and atenololf

References: aDegenhart et al., 2007; bMachelska, 2007; cMahieu-Caputo et al., 2002; dMousa et al., 2007; eRittner et al., 2008; fVerri et al., 2006; gZhang & An,

2007.

159Pediatric Biobehavioral Pain Measures

muscle and cutaneous pain, 2008. They examined

22 healthy adult subjects (11 men, 11 women; aged 19-

49 years). An increase change in signal intensity was

used as their form of measurement, and they observed

that there were gender-based differences in the hippo-

campus, cerebella cortex, midcingulate cortex, and dor-

solateral prefrontal cortex. Women showed increasedsignal intensity which occurred in the cingulate, insular,

primary somatosensory, secondary somatosensory, and

cerebellar cortices during both muscle and cutaneous

pain compared with men. Another study performed on

14 adult subjects (aged 14-40 years), by Owen, Bureau,

Thomas, Prato, and Lawrence (2008), used perfusion

MRI to examine pain-induced changes in cerebral blood

flow. The induced pain consisted of a thermal stimuluson the left hand. They found that this method was effec-

tive for the measurement of chronic pain and observed

changes in the insula, secondary somatosensory, and cin-

gulate cortexes. Functional MRI has great utility but has

limited applicability for real-time assessment of pain

owing to the time involved in making measurements as

well as the limitation that the machine itself poses to

the mobility of the patient.

Chemical Biomarkers of PainSeveral chemical biomarkers for pain have been impli-

cated in the literature (Table 1). Endogenous opioid

neuropeptides (enkephalins, endorphins, dynorphins)

have the ability to dampen the perception of pain

(Rittner, Brack, & Stein, 2008). These actions include

opiate-like activity that is involved in regulation of toler-

ance to pain within the central nervous system. b-Endor-phin is a neuropeptide producedby the pituitary starting

as early as 22 weeks’ gestation. It can be found in

amniotic fluid and fetal blood. Other substancesimplicated in the down-regulation of pain include epi-

nephrine, norepinephrine, serotonin, and g-aminobuty-

ric acid. Some chemical mediators dually implicated in

pain and inflammations include prostaglandins, hista-

mine, serotonin, cytokines, and chemokines (Abbadie,

2005). Chemokines function in activating or modi-

fiying nociceptive transmission. Increasing levels of

interleukin-8, one of the first chemokines studied, are as-sociated with increasing levels of hyperalgesia in rat

models (Cunha, 1991). Studies in humans have found

a positive relationship between spinal fluid levels of

interleukin-8 and back pain (Brisby, 2002). Further re-

search is warranted to delineate possible confounding

variables affecting the ultimate pain response.

b-Endorphins have been associated with pain and

stress response (Rittner et al., 2008). In addition, amni-otic fluid b-endorphin (AFBE) levels were studied as

a possible prognostic predictor of degree of intestinal

damage in fetuses with gastroschisis, which causes se-

vere pain response (Mahieu-Caputo et al., 2002). The

intent was to find a relationship between the level of


b-endorphin and postnatal morbidity. Postnatal mor-

bidity was higher when AFBE exceeded 10 mg/L.That is, higher levels of AFBE were associated with

more severe cases of gastroschisis. Researchers believe

that the endorphin production is a result of prenatal

stress and/or pain from bowel injury (Mahieu-Caputo

et al., 2002). Limitations of this study include the rela-tively small sample size (13 infants with gastroschisis

versus 33 infants without gastroschisis). One must

weigh the limited benefit versus the risk of potentially

causing more fetal harm with repeated invasive studies

throughout the pregnancy. In summary, an increase in

b-endorphin may be associated with increased pain re-

sponse caused by injury, such as gastroschisis. Further

research is indicated to better delineate the optimalutility of testing amniotic fluid b-endorphin levels and

the impact on clinical outcomes after delivery.

A double-blind randomized trial compared the

analgesic effectiveness of continuous infusion opioid

versus intermittent bolus infusion of opioid in the

#36-month-old postsurgical population (n ¼ 204)

(Bouwmeester, Anand, van Dijk, Hop, Boomsma, &

Tibboel, 2001). Plasma concentrations of biologic var-iants (lactate, glucose, insulin, norepinephrine, and

epinephrine) known to be elevated in pain response

were measured at five time points (before surgery, at

end of surgery, and 6, 12, and 24 hours after surgery).

Presurgical levels of epinephrine were found to be

higher than postsurgical levels of epinephrine. Eleva-

tion in biologic variables (lactate, glucose, insulin, nor-

epinephrine, and epinephrine) was compared withpain assessment scales (visual analog scale and com-

fort). The two opioid treatment groups showed no sig-

nificant difference in pain response as measured by the

pain scales and the biologic variants. Further conclu-

sions included difference in surgical stress response

in neonates compared with older age groups. After sur-

gery, neonates showed higher glucose levels, lower

mean increases in epinephrine and norepinephrine,and higher insulin levels compared with older age

groups. Implications for further research include op-

portunities to compare and determine efficacy of other

analgesic interventions to assist in determining best

practice. Further study is warranted to examine the

variations in pain responses related to varying chrono-

logic age.

One deterrent to using biomarker levels as a unidi-mensional tool to assess pain is their concurrent rela-

tionship with inflammation and/or stress response.

Mousa, Straub, Schafer, and Stein (2007) found that

the amount of opioid receptors and endogenous opi-

oid agonists (b-endorphin and metenkephalin) corre-

lated with level of inflammation associated with

arthritis. Synovial fluid samples were subjected to

double immunohistochemical analysis of opioid pep-

tides with immune cell markers. The researchers found

that b-endorphin and metenkephalin were expressed

by macrophage-like cells within synovial lining layers.

Overall, b-endorphin and metenkephalin were more

prevalent in patients with rheumatoid arthritis than

in patients with osteoarthritis or joint trauma. Thisstudy further supports the relationship between in-

flammation and pain response.

The potential role of cytokine measurement in

pain assessment is limited by the potential difficulty

in collecting samples without causing serious harm

to the patient. Many of the cytokines are located within

the dorsal root ganglia or spinal cord or within the

tissues surrounding nerves and the site of injury(Zhang & An, 2007). The potential benefit of assessing

chemical biomarkers of pain appears to be in further-

ing our knowledge of the neurobiology of the pain re-

sponse. An understanding of the pathophysiologic

responses of the human body to painful stimuli may al-

low for the development of improved multidimen-

sional pain assessment tools.

Behavioral Measures of PainThe ASPMN guidelines (Herr et al., 2006) recommend

several clinical tools for use on ‘‘infants and preverbal

toddlers’’ and ‘‘pediatric intubated and/or unconscious

persons.’’ Table 2 presents these scales for the nonver-

bal behavioral assessment tools for pediatric patients.

Furthermore, the Pediatric Initiative on Methods, Mea-

surement, and Pain Assessment in Clinical Trials identi-

fied measures to use in pediatric pain clinical researchtrials (Cohen, Lemanek, Blount, Dahlquist, Lim,

Palermo, Mckenna, & Weiss, 2008). Those authors as-

sessed the validity of some clinical pain assessment

tools and suggested to select pain tools according to

the purpose and context of the setting.

The three approaches to measure pain include

self-report, behavioral, and physiologic. Self-report is

considered to be the gold standard of pain assessment(Schiavenato & Craig, 2010). In one study comparing

nurses’ pain ratings using the Face, Legs, Activity, Cry,

and Consolability (FLACC) scale (Merkel, Shayevitz,

Voepeol-Lewis, Malviya, 1997) with those of patients’

pain rating using the Wong-Baker FACES scale, no cor-

relation between the two scales (r ¼ 0.254; p ¼ .381)

were found in patients <5 years old (Willis, Merkel,

Voepel-Lewis, & Malviya, 2003). However, there wasa significant and positive correlation in children 5-7

years old (r ¼ 0.830; p ¼ .0001) demonstrating that

self-report should be used to validate pain if the target

population is developmentally capable of rating its

own pain (Willis et al., 2003).

TABLE 2.

Pediatric Behavioral Pain Scales

PainAssessment

Tool ContentAge

GroupDescriptionof Study

ScoringMeasures

No. ofSubjects Country Validity Reliability

FLACCMerkel,Shayevitsz,Voepel-Lewis,& Malviya(1997)

B 2 mo to 7 y Observed painafter varioussurgicalprocedures inPACU

5 behavioralitems: F, face;L, legs; A,activity; C,cry; C,consolability;each equallyweighted from0 to 2, score0-10

89: 30 IR, 29analgesiceffect, 30concurrentvalidity

USA Concurrentvalidity: r ¼ .80;p < .001(against OPS);constructvalidity:‘‘significantly’’higher atpreanalgesiathan at 10, 30,and 60 min(p < .001)

IR: kappa: range0.52-0.82(measuredeachassessmentcategoryseparately)

COMFORTAmbuel, Hamlett,Marx, & Blumer(1992)

B & P Infants(newbornto 204 mo)

Assessed level ofdistress onventilatedchildren inPICU

6 behavioralmeasures:alertness,calmness,muscle tone,movement,facialexpression,respiratoryresponse; 2physiologiccomponents:HR, MAP; 1-5points for each,score 8-40

37 USA Concurrentvalidity0.26-0.90,overall 0.75(against VAS)

IR: r 84, range0.51-0.93(kappa); IC:

Cronbach a 0.90

COMFORTVan Dijk et al.(2001)

B & P 0-3 y Assessed painafter majorabdomen orthoracicsurgery inPSICU

6 behavioralmeasures and 4physiologiccomponents:HR, MAP, HRV,MAPV; score8-40

204 Netherland CorrelationbetweenCOMFORT‘‘behavioral’’and 4physiologicitems: 0.44,0.48, 0.37, 0.49

Not tested

(Continued )

161

Pediatric

BiobehavioralPain

Measures

s

TABLE 2.Continued

PainAssessment

Tool ContentAge

GroupDescriptionof Study

ScoringMeasures

No. ofSubjects Country Validity Reliability

DSVNIDistress Scale forVentilatedNewbornInfants (original)

Sparshott (1996)

B & P Newborninfants

Assessedreaction topain/distresson ventilatedchildren

3 behavioralitems: facialexpression(0-3), bodymovement (0-3), color (0-2);4 physiologicchanges: HR,blood pressure,oxygenation,temperaturedifferential;behavioralscore 0-8, noscoring onphysiologic

N/A UK Assessmentcategoriesselected fromliterature review

Not tested

CRIESCrying, RequiresIncreasedOxygenAdministration,Increased VitalSigns,Expression,Sleeplessness(original)

Krechel & Bildner(1995)

B & P Neonates Assessed pain 3 behavioral and2 physiologicmeasures: C,crying; R,requiresincreasedoxygenadministration;I, increasedvital signs; E,expression; S,sleeplessness;score 0-10

24 USA Concurrentvalidity 0.72(against VAS)

IR 0.72

CHIPPSChildren’s andInfants’PostoperativePain Scale(original)

Buttner & Finke(2000)

B Newbornto 1.5 y

Assessed pain inthe firstpostoperativehours

5 behavioralmeasures:crying, facialexpression,posture of thetrunk, postureof the legs,motorrestlessness

584 Germany Sensitivity 97%,specificity 86%

IR 0.93; IC:Cronbach a:0.92 toddler,0.96 infants

B¼ behavioral; HR¼ heart rate; HRV¼ heart rhythm variability; IC¼ internal consistency; IR¼ interrater reliability; MAP¼mean arterial pressure; MAPV¼mean arterial pressure variability; OPS¼ objective pain

scale; P ¼ physiologic; PACU ¼ postanesthesia care unit; PICU ¼ pediatric intensive care unit; PSICU ¼ pediatric surgery intensive care unit; VAS ¼ visual analog scale.

162

Arif-R

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TABLE 3.

Facial Expression Correlated with Pain by Using Facial Action Coding Systems

Description

Action Unit Facial Action Coding System Child Facial Coding System Neonate Facial Coding System

1 Inner brow raise Brow lower Brow bulge2 Outer brow raise Squint Eye squeeze4 Brow lower Eye squeeze Nasolabial furrow deepen5 Upper lid raise Nose wrinkle Open mouth6 Cheek raiser Nasolabial furrow Vertical stretch mouth7 Lid tightener Cheek raise Horizontal stretch mouth10 Upper lip raiser Upper lip raise Chin quiver12 Lip corner puller Lip corner pull Taut tongue17 Chin raiser Vertical mouth stretch Tongue protrusion18 Lip pucker Horizontal mouth stretch20 Lip stretch Blink23 Lip tightener Flared nostril24 Lip presser Open lips25 Lip part26 Jaw drop28 Lips suck45 Blink43 Eyes closed


Unfortunately, pain assessment is difficult in nonver-bal pediatricpatients such asneonates, infants, preverbal

toddlers, and intubated and/or unconscious cognitively

impaired patients. Nonverbal pediatric patients are un-

able to communicate pain or discomfort, because of lan-

guage, cognitive, developmental, or physiologic issues

(Breau, Camfield, McGrath, & Finley, 2004; Cohen

et al., 2008; Herr et al., 2006; Johnston, 1993; McGrath,

Rosmus, Camfield, Campbell, & Hennigar, 1998). Inthese contexts, observational methods that focus on

nonverbal behavior, including indices of facial, vocal,

and motor behaviors and physiologic measures, have

been identified.

Facial ExpressionsFacial expression is considered to be a more stable and

valid component for assessing acute and short-termpain (Breau, McGrath, Craig, Santor, Cassidy, & Reid,

2001; Craig, Hadjistavropoulos, Grunau, & Whitfield,

1994; Grunau & Craig, 1987). There are a number of

behavioral assessment tools developed to capture

facial expression (Table 3). The Facial Action Coding

System (FACS), developed by Ekman and Friesen

(1978), identifies facial expressions specific to pain

that have shown evidence for validity and reliability inadults and children (Craig, 1998; Craig et al., 1994;

Craig & Patrick, 1985; Oberlander, Gilbert, Chambers,

O’Donnell, & Craig, 1999). The FACS describes 44

specific facial muscle movements or action units

(AUs). The facial action units are typically identified

through the use of slow-motion stop-frame feedbackvideo to determine the presence and absence of

discrete facial actions. In a study by Larochette,

Chambers, and Craig (2006), the investigators used

the FACS to identify genuine, suppressed, and faked

facial expressions of pain in 50 healthy 8–12-year-old

children. They identified 18 AUs related to pain re-

sponse (Table 3). The interrater reliabilities for overall

frequency and intensity of AUs were 0.95 and 0.79, re-spectively. The results indicated that more frequent

and more intense lip corner puller (AU12), cheek raiser

(AU6), and lid tightened (AU7)were displayedwhen ex-

posed to cold water as a pain stimulus.

The Neonatal Facial Coding System (NFCS) devel-

oped by Grunau and Craig (1987) identifies specific

pain facial actions among newborns undergoing heel

lance procedures. Like the FACS, the NFCS assesses dis-crete facial actions using video played back in real time

with stop-frame capability. An expert coder identified

total facial activity and cluster-specific facial features

(brow bulge, eye squeeze, nasolabial furrow, and

open mouth) that have been shown to be significantly

associated with acute and postoperative pain in

infants (Craig, 1998; Craig, Whitfield, Grunau, Linton,

Hadjistavropoulos, 1993; Grunau and Craig, 1990).Figure 1 illustrates some of the common facial actions

corresponding to pain in infants.

Guinsburg, de Ara�ujo Peres, Branco de Almeida,

de C�assia Xavier Balda, C�assia Berenguel, Tonelotto,

and Kopelman (2000) used two pain assessment

FIGURE 1. - Facial expression correlated with pain using the Neonatal Facial Coding System.


methods, the NFCS and the Neonatal Infant Pain Scale

(NIPS) (Lawrence, Alcock, McGrath, Kay, MacMurray,

& Dulberg, 1993). They coded distinct facial activities

that measure pain using NFCS, including presence orabsence of eight facial movements: brow bulge, eye

squeeze, nasolabial furrow deepened, open lips,

mouth stretch, lips pursed, taut tongue, and chin

quiver (1 point for each with a total score of 0-8

points). In addition, they used the NIPS, which is com-

posed of facial expression (0/1 point), cry (0/1/2

points), breathing pattern (0/1 point), position of

arms (0/1 point), position of legs (0/1 point), and stateof arousal (0/1 point). The interrater reliability was es-

tablished between two observers who scored the

NFCS and the NIPS using the number of actions agreed

upon by both observers divided by the number of ac-

tions scored by the two observers. The results indi-

cated interobserver reliability of k ¼ 0.94 for NFCS

and k ¼ 0.93 for NIPS. Furthermore, there was strong

agreement between the two coders for the vast major-ity of NFCS and NIPS items.

Similarly, the Child Facial Coding System (CFCS)

(Chambers, Cassidy, McGrath, Gilbert, & Craig, 1996)

was developed to assess acute pain responses in young

children aged 1-6 years. The CFCS codes 13 discrete

AUs adapted from both the FACS and the NFCS. Be-

cause there are less age-related differences in facial ac-

tivity beyond 1 year of age, CFCS has been used inadolescents to identify pain expressions (Lilley, Craig,

& Grunau, 1997). Breau et al., (2001) studied 123 chil-

dren aged 4-5 years undergoing routine diphtheria, per-

tussis, tetanus, and polio (DPT) immunization. The

purpose of the study was to establish sensitivity of

the CFCS during noxious stimuli. For the study, the

DPT immunization injection was the noxious stimulus.

They identified 13 facial actions, of which six reflected

the children’s acute pain experience. The results indi-cated that AU frequency and intensity for brow lower,

squint, flared nostril, nose wrinkle, lip corner pull, and

vertical mouth stretch occurred more often during im-

munization injection (the needle phase) than before

the injection (preneedle phase; p < .004 [frequency]

and p < .005 [intensity]).

Overall, these FACSs provide a comprehensive de-

scription of the facial expression during painful stimuliwhich could be used to develop better behavioral assess-

ment tools. One major limitation for use of the FACS in

the clinical setting is the extensive training and complex-

ityof coding that is required.Nonetheless, once the facial

expressions are narrowed down, FACS coding could be

used to assess facial expression during pain responses re-

lated to varying pediatric populations.

VocalThere have been cry features that have been exten-

sively studied using spectrographic devices. Short la-

tency to onset of cry, longer duration of the first cry

cycle, higher fundamental frequency, and greater in-

tensity in the upper ranges are pain-specific cry

features in infants and neonates during painful proce-

dures (Grunau, Johnston, & Craig, 1990; Johnsonton& Strada, 1986; Krechel & Bildner, 1995).

In a study by Runefors, Arnbj€ornsson, Elander, andMichelsson (2000), the researchers hypothesized that

a newborn infant’s cry can be used in conjunction

with an instrument to measure pain. They used heel


sticks as noxious stimuli to elicit pain response for phe-

nylketonuria screening in 50 healthy newborn infants.

Their cries of pain were recorded and analyzed acous-

tically with the assistance of a computer program espe-

cially designed for this purpose (Innomess Elektronik,

Berlin, Germany). The sound spectrogram, a well

tested instrument, is a visual diagram of the soundsignal. Time is recorded on the horizontal scale; fre-

quency is recorded on the vertical. The curve of

the lowest harmonic on the spectrogram gives the

fundamental frequency, and the upper lines give the

harmonic overtone multiples of the fundamental

frequency. The analysis showed that the crying sound

after the painful stimulus of the heel prick had a signi-

ficantly higher fundamental frequency and lasted lon-ger at the first cry (2.7 seconds) than at the fifth cry

(0.8 seconds; p < .001). The results indicated that

the first cry was more like a cry of pain, and the fifth

cry more resembled crying for reasons other than

pain. They suggested that newborn infants react to

pain in a recognizable way. However, they also sug-

gested that other stimuli may cause a similar reaction.

The researchers recommended that crying can be usedto measure pain in newborn infants only when the

cause of crying is known. A significant clinical practice

limitation of cry analyses is the need for a specialized

spectrographic apparatus that requires advanced train-

ing. The expense of the training and the apparatus con-

tributes to increased research costs. In addition, not all

infants will cry when in pain, such as patients with en-

dotracheal intubation or physiologic fatigue (Grunauet al., 1990; Johnston & Strada, 1986; van Dijk, Koot,

Abu Saad, Tibboel, & Passchier 2002).

Motor BehaviorsBody movement as a pain indicator focuses on observa-

tion of arm and leg activity. Body movement is included

in many pain assessment tools, but this behavioral

marker changes with development from the neonatal

stage through infancy and into adolescence. Increasedactivity, posture, and tense muscle tone are thought to

indicate more pain in neonates (Hummel & van Dijk,

2006). Muscle tone and breathing pattern take an inter-

mediate position between behavioral and physiologic

indicators (van Dijk et al., 2002). Muscle tone or pos-

ture may reflect tenseness due to abdominal pain but

may also reflect the behavior of a frightened child. Shal-

low and rapid breathing may reflect hyperventilationdue to anxiety or may be caused by pain after thoracic

or abdominal surgery (van Dijk et al., 2002). A major

limitation of assessing body movement is that children

may avoid moving because of pain (van Dijk et al.,

2002); therefore, special attention needs to be paid

to increased or decreased activity from a child’s

baseline.

Physiologic MeasuresPhysiologic measures of pain, which include heart rate,

respiratory rate, oxygen saturation, and blood pres-

sure, have been examined in neonates during acute

pain caused by heel lance (Johnston, Stevens, Yang,

& Horton, 1995) and circumcision (Howard, Howard,& Weitzman, 1994). The benefit of physiologic mea-

sures for pain assessment has been described by

Sweet and McGrath (1998) but it has been debated be-

cause of lack of specificity for pain (van Dijk, de Boer,

Koot, Duivenvoorden, Passchier, Bouwmeester, &

Tibboel, 2001). Fluctuations in heart rate, blood pres-

sure, and oxygen saturation may be influenced by

poor circulation due to blood loss, fluid intake, bodytemperature, and medical interventions. Several stud-

ies have concluded that physiologic pain indicators

are not ideal to assess pain and recommend that the

pain assessment tools be based on behavioral pain indi-

cators (Buchholz, Karl, Pomietto, & Lynn, 1998;

Buttner & Finke, 2000; McGrath & Unruh, 1994).

In a study by van Dijk et al. (2001), the researchers

examined the association between physiologic and be-havioral pain measures using the COMFORT scale in

children. The COMFORT scale consists of both behav-

ioral and physiologic components. The behavioral

components are described further in Table 2. Physio-

logic measures included mean arterial pressure, heart

rate, heart rate variability, and mean arterial pressure

variability. The researchers studied 204 subjects and

found that as children between 0 and 3 years old in-crease in age, their respiratory and heart rates decrease

and their overall blood pressure increases in response

to postoperative pain. That study also found moderate

correlations between crying and heart rate as well as

between facial expressions and heart rate variability

in nonverbal children. A low correlation between the

physiologic measures made during the study seems

to indicate that the measurements were independentof each other. Intermittent noninvasive measuring of

heart rate and blood pressure could induce distress

or anger in infants and children, which would increase

the unreliability of such pain indicators (van Dijk,

2001).

In summary, the means for validating the pain as-

sessment tools are provided in Table 2. Although all

of the tools have behavioral components, the Crying,Requires Oxygen, Increased Vital Signs, Expression,

and Sleep (CRIES) scale (Krechel & Bildner, 1995)

and the COMFORT scale are the only ones that contain

both physiologic and behavioral measures of pain. The

correlations of the physiologic measures are lower on


the studies that tested with the COMFORT scale

(Ambuel, Hamlett, Marx, & Blumer, 1992; van Dijk,

de Boer, Koot, Tibboel, Passchier, & Duivenvoordent,

2000). Ambuel et al., (1992) pointed out that heart

rate and arterial blood pressure had the lowest inter-

rater reliabilities due to the way they were measured.

The researchers predict that the inter-rater reliabilitywould increase if the physiological measures are ob-

served for two minutes and the trend is measured

(Ambuel et al., 1992). In addition, van Dijk et al.

(2000) pointed out the limited validity of heart rate

and mean arterial pressure as a measurements of pain

and suggested the need for further research with clin-

ical data to support these measures, because they are

frequently used as indicators of pain in clinical settings.However, from a research perspective, the physiologic

measures may or may not be appropriate depending on

the specific pediatric population.

CONCLUSIONS

Assessment of pain in the noncommunicative pediatric

population provides many challenges for health careproviders and researchers. Results of the present liter-

ature review indicate many avenues for future studies,

including validation in the pediatric population. Clini-

cal implications of the use of objective markers for

pain measurement in the noncommunicative pediatric

patient may include improved individualized titration

of analgesia, decreased physiologic stress response

from inadequate analgesia, and avoidance of chronic

pain conditions secondary to inadequate management

of acute pain. Further research on pain assessment isneeded in the pediatric population by using a variety

of markers for pain. Additional studies of interest in-

clude comparison of chemical and mechanical bio-

markers for pain with validated behavioral markers

for pain in the pediatric population. One such study

may measure the correlation between EEG, serum

b-endorphin, and the FLACC behavioral pain assess-

ment tool during painful stimulus. Implications for fur-ther research include opportunities to improve validity

and reliability of these pain assessment tools by using

advanced methods such as analyses of facial expres-

sion, spectrographic devices, neuromuscular activity,

or chemical markers.

Acknowledgments

The authors thank Cindy Munro, RN, PhD, Professor, Depart-

ment of Adult Health, Virginia Commonwealth University

School of Nursing, for her insightful comments in this litera-

ture review.

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Biobehavioral Measures for Pain in the Pediatric Patient