Pulmonary Critical Care FACIAL EXPRESSION AS AN …ajcc.aacnjournals.org/content/22/5/412.full.pdfpain response, and describe the effect of patient factors on ... Mamoona Arif Rahu

By Mamoona Arif Rahu, RN, PhD, CCRN, Mary Jo Grap, RN, PhD, ACNP, Jeffrey F. Cohn,PhD, Cindy L. Munro, RN, PhD, ANP, Debra E. Lyon, RN, PhD, FNP-BC, and Curtis N.Sessler, MD

Background Facial expression is often used to evaluate painin noncommunicative critically ill patients.Objectives To describe facial behavior during endotrachealsuctioning, determine facial behaviors that characterize thepain response, and describe the effect of patient factors onfacial behavior during pain response.Methods Fifty noncommunicative patients receiving mechanicalventilation were video recorded during 2 phases (rest and endo-tracheal suctioning). Pain ratings were gathered by using theBehavioral Pain Scale. Facial behaviors were coded by usingthe Facial Action Coding System for 30 seconds for each phase.Results Fourteen facial actions were associated more withendotracheal suctioning than with rest (z=5.78; P< .001). Thesum of intensity of the 14 actions correlated with total meanscores on the Behavioral Pain Scale (r=0.71; P< .001) andwith the facial expression component of the scale (r=0.67; P< .001) during suctioning. In stepwise multivariate analysis, 5 pain-relevant facial behaviors (brow raiser, brow lower, nosewrinkling, head turned right, and head turned up) accountedfor 71% of the variance (adjusted R2 = 0.682; P< .001) in painresponse. The sum of intensity of the 5 actions correlated withtotal mean scores on the behavioral scale (r=0.72; P< .001)and with the facial expression component of that scale (r=0.61;P< .001) during suctioning. Patient factors had no associationwith pain intensity scores.Conclusions Upper facial expressions are most frequentlyactivated during pain response in noncommunicative criticallyill patients and might be a valid alternative to self-report ratings.(American Journal of Critical Care. 2013;22:412-422)

FACIAL EXPRESSION AS AN

INDICATOR OF PAIN IN

CRITICALLY ILL INTUBATED

ADULTS DURING

ENDOTRACHEAL SUCTIONING

412 AJCC�AMERICAN JOURNAL OF CRITICAL CARE, September 2013, Volume 22, No. 5 www.ajcconline.org

©2013 American Association of Critical-Care Nursesdoi: http://dx.doi.org/10.4037/ajcc2013705

Pulmonary Critical Care

by AACN on May 18, 2018http://ajcc.aacnjournals.org/Downloaded from

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The Facial Action Coding System (FACS)25,26 is acomprehensive system for recognizing the muscularactivity in facial appearances. Action units representthe movements of facial muscles, and units associatedwith pain in healthy volunteers have been identi-fied27-37 (Table 2). Frequently reported pain-relatedfacial actions include lowered brows, raised cheeks,tightened eyelids, a raised upper lip or openedmouth, and closed eyes.26-39 FACS has been used tounderstand facial expressions in infants, children,and adults, including the elderly, but little empiricevidence exists about use of the system in noncom-municative critically ill adults. Indeed, behaviorsstill cannot be associated with pain in noncommu-nicative patients. However, facial expression is com-monly used to evaluate pain in these patients.

Therefore, the specific aims of this prospectivestudy were to describe facial actions during endotra-cheal suctioning in noncommunicative critically illpatients, determine facial actions that may charac-terize the pain response, and describe the effect ofpatient factors (eg, age, sex, race, diagnosis, duration

of endotracheal intubation, length of stay in theintensive care unit [ICU], use of analgesics and seda-tives, sedation level, and severity of illness) on facialaction during the pain response.

Methods Setting and Sample

The sample consisted of 50 patients who werenoncommunicative (unable to use speech, writtennotes, or eye or hand motions), intu-bated, and receiving mechanical ven-tilation in an adult surgical-traumaand a medical ICU at Virginia Com-monwealth University Health System,Richmond, Virginia. Patients wereexcluded if they had persistent neu-romuscular disorders, head trauma,or stroke or were receiving neuro-muscular blockers because these conditions mightaffect facial expressions and study measurements.

Measurement of Key VariablesPain Level. Pain levels were measured by using

the Behavioral Pain Scale (BPS)19 commonly usedin intubated patients.7,19,40 An interrater reliability ofk=0.90 between the principal investigator (M.R.)and another expert clinical nurse was establishedduring routine patient care before the study began.

Facial Action. Facial actions were evaluated byusing the FACS. FACS scores have been highly reli-able in a variety of studies (Table 2) and indicate adistinct pattern of facial actions characteristic ofpain.27-39 The basic elements of FACS action unitscan be reliably identified by trained FACS coders.Coding was performed by a certified FACS coder(M.R.). A second coder also certified in FACS cod-ing established interrater reliability by scoring 10%of the randomly selected videos (246 frames) duringthe endotracheal suctioning. Interrater reliability,

Critically ill patients experience acute pain that may be associated with routinecare or their underlying diseases.1-5 Pain assessment is difficult in patients whocannot communicate their pain level by using speech, written notes, or eye orhand motions.3,6,7 Assessment of pain in these noncommunicative patients hasno gold standard.8-13 Frequently used pain assessment tools10-15 consist of behav-

ioral dimensions (facial expression, body movement, verbal response, ventilator compliance)but include a variety of facial descriptors that are used interchangeably (eg, wincing, frown-ing, grimacing)1,16-23 (Table 1). However, disagreement in rating the facial component has beenreported.24 In order to optimally evaluate pain, a comprehensive analysis of facial expressionin critically ill noncommunicative patients is needed.

About the AuthorsMamoona Arif Rahu is a clinical nurse specialist in Critical Care, Cindy Munro was, at the time of thisresearch, and Mary Jo Grap is a professor in AdultHealth and Nursing Systems, and a Nursing AlumniEndowed Professor, and Debra E. Lyon is an associateprofessor and chair, Family and Community Health Nurs-ing, School of Nursing, Virginia Commonwealth University,Richmond, Virginia. Curtis N. Sessler is a professor ofmedicine and director, Center for Adult Critical Care,Division of Pulmonary and Critical Care Medicine, Depart-ment of Internal Medicine, School of Medicine, VirginiaCommonwealth University, and Jeffrey F. Cohn is aprofessor of psychology and director of the Affect Analy-sis Group, Department of Psychology, University ofPittsburgh, Pittsburgh, Pennsylvania.

Corresponding author:Mamoona Arif, RN, PhD, CCRN, VirginiaCommonwealth University, 808 Stonemeadow Dr, GlenAllen, VA 23060 (e-mail: [email protected]).

www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, September 2013, Volume 22, No. 5 413

There is disagreementabout ratings offacial behaviorsduring pain.




alert) to +4 (combative). The scale has been validatedagainst a visual analogue scale of sedation and agi-tation and tested for interrater reliability in adultICUs.44-46 Interrater reliability (k=1.0) was estab-lished between the principal investigator (M.R.) andanother expert clinical nurse during routine patientcare before the study began.

Endotracheal Suctioning. Endotracheal suctioningwas used to elicit a pain response because of its valid-ity as a noxious event.1,47-54 In a recent study,5 755patients who could self-report pain indicated greaterpain during endotracheal suctioning (mean, 4.0; SD,3.3) than before suctioning (mean, 2.1; SD, 2.8). Themost frequently observed pain behavioral responsesduring endotracheal suctioning were grimace (52%),clenched fists (24%), rigidity (23%), and wince (22%).

ProceduresThe study was approved by the appropriate insti-

tutional review board, and consent for participation

determined by using the Ekman-Friesen formula,26

was 0.88 with k=0.70, indicating strong agreementbetween the 2 raters.

Patients’ Characteristics. Data on age, sex, race andethnic background, diagnosis (reflecting type of crit-ical illness and population; ie, surgical or medical),duration of endotracheal intubation, length of stay(from date of ICU admission to date of enrollment),and total amount of sedatives and analgesics usedduring the 24 hours before enrollment were collectedfrom the medical records. Doses of opioids andbenzodiazepines were converted to fentanyl andlorazepam equivalents, respectively, as described byCammarano et al.41 Severity of illness was documentedon the basis of the 24 hours before enrollment byusing the Acute Physiology and Chronic HealthEvaluation III.42,43

Sedation level was measured by using the Rich-mond-Agitation Sedation Scale (RASS),44 a 10-pointscale, ranging from -5 (unarousable) to 0 (calm and

414 �AJCC�AMERICAN JOURNAL OF CRITICAL CARE, September 2013, Volume 22, No. 5 www.ajcconline.org

Table 1 Pain measurement tools and facial behaviordescriptors for noncommunicative patients

Behavioral Pain Rating Scale (BPRS) Mateo and Krenzischek17

(1992; English version) Persson and Ostman18

(2004; Swedish version)

The Pain Assessment and InterventionNotation (PAIN) algorithm

Puntillo et al16 (1997)

Behavioral Pain Scale (BPS) Payen et al19 (2001)

Nonverbal Pain Scale (NVPS) Odhner et al20 (2003)

Pain Behavior Assessment Tool (PBAT) Puntillo et al1 (2004)

Critical-Care Pain Observation Tool (CPOT) Gélinas et al21 (2006; French version) Gélinas, et al22 (2007; English version)

Does not frown forehead or grimaceSlight frowning and grimacingModerate frowning and grimacingConstant frowning and grimacing

Grimacing, frowning, wincingDrawn around mouth and eyesWrinkled foreheadTeary/crying

Relaxed Partially tightened (eg, brow lowering) Fully tightened (eg, eyelid closing) Grimacing (eg, folded cheeks)

No particular expression or smileOccasional grimace, tearing, frowning, wrinkled foreheadFrequent grimace, tearing, frowning, wrinkled forehead

Grimace FrownWince Eyes closed Grin/smileEyes wide open with eyebrows raised Unable to assessLooking away in opposite direction of the pain Mouth wide open to expose teeth and tongueClenched teeth exposing slightly open mouthNone Other

Relaxed, neutral: no muscular tension observedTense: presence of frowning, brow lowering, orbit tightening, and

levator contractionGrimacing: all of the preceding facial movements plus eyelid tightly

closed

0123

1234

012

01

2

Scale/reference ScoreFacial behavior descriptors and scoring




in the study was obtained from each patient’s legallyauthorized representative. Routine suctioning wasperformed by the nursing staff according to eachpatient’s clinical need.

Video recordings for FACS coding were obtainedby using a digital camcorder (Canon GL2) zoomedto the patient’s face and neck. The videos were ana-lyzed at a later time for 2 phases: when the patientappeared most comfortable (baseline) and duringthe endotracheal suctioning. The time segment forFACS coding was standardized to 30 seconds foreach phase. This time frame was based on prelimi-nary findings that suctioning episodes in this set-ting ranged from 6 to 28 seconds (mean, 13.33;SD, 4.8). On the basis of the criteria establishedby the developers of FACS,26 each 30-second phasewas coded separately for all possible action unitsfor their frequency of occurrence, duration ofexpression (in seconds), and intensity of expres-sion (on a 5-point scale). The BPS and RASS scoreswere recorded at baseline and during the endotra-cheal suctioning.

Data AnalysisData were analyzed by using Observer XT 8.0

Software (Noldus Information Technology) andJMP 10.0 Statistical Software (SAS Institute).Descriptive statistics and the Wilcoxon signed ranktest were used to determine the relationshipbetween action units activated during baseline andthose activated during endotracheal suctioning.Stepwise multivariate analysis was used to developa model that best described the FACS pain scorebased on pain-relevant facial action units.32-33,36,37

Spearman rank correlation values were used todescribe the relationship between BPS scores, RASSscores, and patient factors on facial action duringthe pain response for a < 0.05.

ResultsPatients’ Characteristics

The sample consisted mostly of men and wasevenly divided between African Americans andwhites. The mean age was 52.5 years (Table 3). Theprimary reason for ICU admission was respiratory


Table 2 Studies of facial action units associated with pain in adults

Craig and Patrick27 (1985)

Patrick et al28 (1986)

Prkachin29 (1992)

Wilkie30 (1995)

Hadjistavropoulos et al31

(2000)

Hadjistavropoulos et al32

(2002)

Kunz et al33 (2004)

Lints-Martindale et al34

(2007)

Kunz et al35 (2007)

Kunz et al36 (2008)

Prkachin and Solomon37

(2009)

72 college students; mean age 18.65 (SD, 1.58) y

30 women; age range, 17-28 y

41 college students; mean age 20 (SD, 2.02) y

43 adult outpatients with lung cancer

58 frail elders with cognitive impairmentafter hip replacement; mean age 76.6(SD, 8.1) y

82 patients after surgical knee replacement;mean age 73.1 (SD, 7.6) y

40 college students; mean age 24 (SD, 3.2) y

27 patients with Alzheimer disease; meanage 78 (SD, 4) y; 36 patients with no cog-nitive impairment; mean age 78 (SD, 4) y

42 patients with dementia; mean age 76.7(SD, 7.3) y; and 54 healthy controls; meanage 74.2 (SD, 5.6) y

40 college students; mean age 24.1 (SD, 3.2) yand 61 elderly students; mean age 72.3(SD, 5.6) y

129 patients with shoulder pain; mean age42.23 (SD, 14.48) y

6, 7, 10, 12, 25, 26, 27, 43, 45

4, 6, 10, 45

4, 6, 7, 9, 10, 43

4, 6, 7, 9, 10, 20, 26, 27, 43

1, 2, 4, 6, 7, 9, 10, 12, 17, 18,20, 24, 25, 26, 27, 43, 45

1, 2, 4, 6, 12, 17, 18, 20, 24,25, 26, 43, 45

1, 2, 4, 6, 7, 9, 10, 12, 17, 25,26, 27, 45

4, 7, 25, 26, 43, 45, 61, 62,63, 64, 73

1, 2, 4, 6, 7, 9, 10, 17, 25, 26,27, 45

1, 2, 4, 6, 7, 9, 10, 12, 14, 25,26, 27, 43, 45

4, 6, 7, 9, 10, 12, 20, 25, 26,27, 43

Cold pressor test

Electric shock

Electric shock, cold pressor test,mechanical pressure, muscleischemia

Activity protocol—sit, walk,stand, recline

Sit, stand, walk, and recline

Reclining, standing, knee bending

Electrical shock and mechanicalpressure

Electrical-thermal and mechanicalpressure

Mechanical pressure

Electrical shock and mechanicalpressure

Passive range of motion

Study Action unitsaProcedurePopulation

a See Table 4, Ekman and Friesen,25 and Ekman et al26 for explanations of the numbers.




failure. Patients from the 2 ICUs did not differ indemographic characteristics (Table 3). A moderatecorrelation was detected between age and score onthe Acute Physiology and Chronic Health Evalua-tion III (r=0.39; P= .005). An inverse relationshipwas detected between age and fentanyl equivalents(r=0.53; P< .001). Patients with longer durationof intubation had longer lengths of stay in the ICUthan did patients with shorter durations (r=0.78; P< .001).

Pain LevelAccording to BPS scores, pain level was higher

during endotracheal suctioning than at baseline(F99 =123.89; P< .001). At baseline, the facialexpression component of the BPS indicated that92% of the patients (n=46) had “relaxed” facialexpressions, and the overall mean BPS score was3.28. During endotracheal suctioning, 46% of thepatients had facial expressions that were “partiallytightened” 24% had “fully tightened expressions,”and 18% were “grimacing”; the total mean BPSscore was 6.36. Total mean BPS scores correlatedwith total mean RASS scores (r = 0.60; P < .001).

Description of Facial ActionsThe Wilcoxon signed rank test indicated that

activation of 14 action units differed significantlybetween baseline and endotracheal suctioning(Table 4). The Figure illustrates the action unitsactivated at baseline and during endotracheal suctioning.

Facial Actions and Pain ResponseThe 14 facial actions varied in frequency, dura-

tion, and intensity of correlation with total meanscores on the BPS (Table 5). For example, the fre-quency, duration, and intensity of brow lower (actionunit 4) had moderate to strong correlation with thetotal mean BPS scores. Results of the Spearman rankcorrelation were r=0.30 for frequency (P= .03),0.63 for duration (P< .001), and 0.74 for intensity(P< .001). Patients tended to turn their heads moreto the right side of the bed, and the frequency, dura-tion, and intensity of this finding had a positivecorrelation with total mean BPS scores. Endotrachealtubes were located on the right side of the mouthin 27 patients, on the left side in 18, and in themiddle in 3. Two patients had a tracheostomy. Morepatients tended to turn their heads to the right (32%)than to the left (22%). No significant relationshipwas detected between location of the endotrachealtube and head turning. However, frequency, dura-tion, and intensity of cough correlated with head

Table 3 Characteristics of sample and major variables (N= 50)

Sexa

Male Female

Ethnicitya

Black or African American, not Hispanic White, not Hispanic American Indian or Alaskan native Asian

Intensive care unita

Medical Surgical/trauma

Diagnosis or reason for admission Respiratory failure Surgery Transplant Motor vehicle accident Septic shock Other

Endotracheal tube suctioningb

Once Twice

Age,a y

Duration of intubation,c d

Stay in intensive care unit,d d

Suctioning duration, s

Score on Acute Physiology and Chronic Health Evaluation III

Opioidse

Fentanyl, µg Morphine, mg Hydromorphone, mg Fentanyl equivalents unit, mg

Benzodiazepinee

Lorazepam, mg Midazolam, mg Lorazepam equivalents unit, mg

Othere

Propofol, mg Dexmedetomidine, µg

Score on Behavioral Pain Scalef

BaselineProcedure

Score on Richmond Agitation- Sedation Scale

BaselineProcedure

5248

4848

22

5446

5024

810

44

8416

18-85

1-17

1-17

5.99 - 28.13

37-140

0 - 49100 - 750 - 720 - 8.4

0 - 200 - 268

0 - 89.33

0 - 83040 - 3600

3-53-11

-5 to + 2-5 to + 2

3-3 5-8

-4 to -1-4 to -1

3.06.0

-3.0-2.5

17.2

3.9

3.7

8.1

26.0

1316.5110.7710.661.56

4.0066.5823.07

1689.0578.3

52.5

5.1

5.74

13.33

92.8

1662.121.861.961.78

1.0253.4818.85

659.5113.0

2624

2424

11

2723

2512

4522

428

Abbreviation: IQR, interquartile range.a No significant difference.b Number of times suctioning was performed during 30-second segment.c From day of intubation to the time of study enrollment.d From day of admission to intensive care unit to the time of study enrollment.e Total dosage given in past 24 hours.f P< .001.

Variable

Range

RangeIQRMedian

SDMean

%Frequency





movement (action units 52, 53, and 57; r=0.35 (P= .01), 0.30 (P= .04), and 0.49 (P< .001).

In order to evaluate which action units werepredictors of pain, all 14 action units were enteredinto a stepwise model. The final model included 5pain-relevant facial action units that accounted for71% of the variance (adjusted R2 =0.682) for pre-diction of pain response (F49=21.99; P< .001). Theseaction units included inner brow raised, brow lower,nose wrinkle, head turn right, and head turn up.

Per the convention established by Prkachin andSolomon,37 intensities were added to define theFACS pain intensity score (Table 6).

On the basis of the 5-point intensity scale usedto code each action unit, the possible FACS painintensity score ranged from 0 to 25. The score washigher during the endotracheal suctioning than atbaseline (mean difference=42.22; z=7.67; P< .001).In addition, the score was strongly correlated withthe mean BPS score (r=0.72; P< .001) and the


Table 4 Activation of facial action units during baseline and noxious procedure (N=50)

Upper part of face

Inner brow raised Outer brow raised Brow lower Upper lid raised Cheek raised Lid tightened Eyes closureBlink

Head position

Head turn left Head turn right Head turn up Head tilt left Head forward

Eye position

Eyes rightEyes up

Lip parting and jaw opening

Lips parted Jaw drop

Lower part of face

Nose wrinkle Lower lip depress Chin raiser Lip pucker Lip stretcher Lip presser

Miscellaneous

Tongue show Jaw clencherBlowPuff

Nasal dilatation Head shake back and forth

Total number of action units activated

<.001.02

<.001.33.001

<.001.009.02

.27

.004<.001

.33

.008

.33

.08

.006

.05

<.001.16.001.05.17.31

.31

.33

.33

.33

.004

.33

<.001

3.492.276.990.983.255.292.612.29

1.112.855.080.982.65

0.981.74

2.751.94

3.491.413.281.951.391.01

1.010.980.980.982.920.98

7.45

3.793.155.301.003.705.493.883.50

3.493.504.621.003.02

1.001.71

5.294.93

3.151.413.392.572.191.97

1.971.001.001.002.731.00

5.78

13.227.14

37.10.98

12.0429.0610.14

8

3.889.98

23.460.988

0.982.98

14.549.58

10.981.98

11.153.041.98

1.980.980.980.987.980.98

43.06

3120885

25141

8248

1020431

11

27

6241

152

23893

3111

321

736

22803

295617

93301

00

3618

001111

100000

192

1245c

67

4345

51525355c

57

62c

63c

2526

916c

171820c

24c

19c

31c

33c

34c

3884c

a Pain-related action units are marked in boldface as reported in previous studies.b Significant results are marked in boldface. c Action units occurring in 5% or less for all 50 patients in the 2 phases were eliminated from subsequent consideration because of the rarity of occurrence.

Namea Number PbZStandard errorof difference

Score, meandifferenceProcedureBaseline

Wilcoxon test (rank sum)No. of times activated

Facial action unit




and able to briefly awaken with eye contact or move-ment to voice but were unable to follow commands.

Facial Actions During Pain ResponsePrkachin and Solomon37 identified 4 core facial

actions that provide the majority of pain informa-tion: brow lower, orbit tightening, nose wrinkling,and eye closure. Various methods (ie, experimentalpain or clinical pain; Table 2) have been used to testthese expressions in healthy volunteers. Our studyextended that research by determining facial expres-sion in noncommunicative critically ill patients andusing endotracheal suctioning as the noxious stimu-lus. We found activation of similar facial actions,specifically brow lower, orbit tightening, nose wrin-kling, and eye closure. However, we also found thatbrow raiser, mouth opening, head position, andnasal dilatation often occurred during suctioning.

Core Facial Actions in Noncommunicative Critically Ill Patients

Brow Lowering and Orbit Tightening (Action Units4 and 6 Plus 7). Facial expression of pain occurredmost often in the upper part of the face (brow lowerand orbit tightening), especially for duration andintensity. These action units highly correlated withdescriptors included in the facial domain of the BPS.

facial expression component of the BPS (r=0.61; P< .001) during endotracheal suctioning. Likewise,the sum of intensities of the 14 action units washighly correlated with mean BPS scores (r=0.71; P< .001) and with the facial expression componentof the BPS (r=0.67; P< .001) during the endotra-cheal suctioning.

Facial Action and Patient FactorsNo association was detected between FACS

pain intensity scores and patient factors. However,the FACS pain intensity scores and RASS values hada strong correlation (r=0.55; P< .001). Likewise,the sum of the intensity scores of the 14 action unitswas strongly correlated with RASS values (r=0.59;P< .001) during endotracheal suctioning.

DiscussionThis study was the first one in which compre-

hensive video analysis was used to measure specificfacial muscle activity in noncommunicative criti-cally ill patients during a type of endotracheal suc-tioning known to elicit a pain response. We alsoinvestigated the relationship among facial expres-sion, pain level, sedation level, and other patientfactors. About half of the patients were adequatelysedated, with light to moderate levels of sedation,


Figure Facial action units (AUs) during baseline and noxious procedure.

AU 43 – Eyes closed

AU 25 – Lips parted

AU 43 – Eyes closed AU 4 – Brow lower

AU 6 – Cheek raised

AU 7 – Lid tightened

AU 25 – Lips parted

Baseline Procedure




Specifically, action units 4 and 7 occurred mostoften with higher intensity for levels 2 and 3 of thefacial expression domain. Of note, level 4 (gri-mace) was recently defined as “folded cheek,”55

which includes several action units that were notvisible in our patients because of the tape used tosecure tubes around the mouth and cheeks. Fur-ther studies are need to test these action units todescribe the relationship between folded cheek andgrimace in various populations.

Nose Wrinkle (Action Unit 9). Although nosewrinkle is generally a common expression of pain

reported in otherwise healthier patients, this actionunit occurred infrequently and was not stronglyassociated with endotracheal suctioning. However,detection of nose wrinkle was often compromisedbecause the visibility of the nose bridge was obscuredby the tape holding a nasogastric tube or the endo-tracheal tube in place. Therefore further studies arewarranted to confirm if these expressions occur inpatients who do not have securing devices aroundthe mouth and nose.

Eye Closure (Action Unit 43). Most people closetheir eyes when they experience pain.26-39 The assump-


Table 5 Spearman's rank correlation of facial action units and score on Behavioral Pain Scale forfrequency, duration, and intensity during noxious procedure (endotracheal suctioning)

Inner brow raised

Outer brow raised

1/2 combineda

Brow lower

Cheek raised

Lid tightened

6/7 combineda

Eye closure (AU 43)

Lips parted (AU 25)

Jaw drop (AU 26)

25/26 combineda

Nose wrinkle (AU 9)

Chin raiser (AU 17)

Nasal dilatation

Head turn right

Head turn up

Head turn forward

52/53/57 combineda

Sum of action units

.01

.12

.009

<.001

.004

.004

.003

.92

.004

.02

.004

.29

.27

.89

.01

.09

.35

.05

<.001

0.35

0.22

0.37

0.74

0.40

0.40

0.41

-0.02

0.40

0.34

0.40

0.15

0.16

-0.02

0.36

0.24

0.14

0.28

0.71

.04

.16

.06

<.001

.02

.01

.005

.12

.11

.10

.12

.55

.23

.95

.02

.06

.26

.01

<.001

0.29

0.20

0.26

0.63

0.33

0.35

0.39

-0.22

0.23

0.23

0.22

0.09

0.17

-0.01

0.33

0.26

0.16

0.34

0.49

.04

.19

.09

.03

.06

.29

.09

.91

.01

.07

.006

.59

.28

.97

.02

.29

.30

.03

.004

0.29

0.19

0.24

0.30

0.27

0.15

0.24

0.02

0.35

0.26

0.38

0.08

0.16

-0.01

0.34

0.15

0.15

0.31

0.39

a Following a precedent established by Ekman and Friesen,25 action units were combined to form 1 variable (eg, if both action units occurred 1 time each,the combined variable was given a frequency of 2). Action units 25 and 26 were combined because they represent varying degrees of mouth opening.Action units 1 and 2 represent varying degrees of eyebrow rising and action units 6 and 7 represent degrees of eye orbit tightening. Action units 52, 53,and 57 represent gross movement of the head.

Facial action unit

PCorrelationPCorrelationPCorrelationName Number

IntensityDurationFrequency

1

2

1/2

4

6

7

6/7

43

25

26

25/26

9

17

38

52

53

57

52/53/57

Table 6 Facial Action Coding System pain intensity score

Pain intensity score 2053453 + + + + =

AU 1Inner brow raised

AU53Head turn up

Totalscore

AU 52Head turn right

AU 9Nose wrinkle

AU 4Brow lower

Facial action unit




respiratory distress caused by endotracheal suction-ing is difficult.

Head Position (Action Units 52 Plus 53 and 57).Interestingly, head position (turn right, turn up,and forward) has not been described as an expres-sion of pain in previous studies, but it occurred fre-quently during endotracheal suctioning in our study.All of the patients in our study were supine withthe head of the bed elevated 30º and tended tomove their head back or side to side during endo-tracheal suctioning. Even though head position wasmoderately correlated with pain level, this findingmay have been patients’ attempts to get away fromthe suctioning procedure and may not necessarilyrepresent a pain response. Head movements areoften the only possible movements for ICU patientsimmobilized in bed. Therefore, head position mayrequire observations with other pain stimuli.

Facial Actions During Pain and Patient FactorsOur findings are also consistent with those of

previous studies in which frequency, duration, andintensity of facial expression did not differ bysex29,56-59 or age.36 Patients who had greater levels ofarousal showed greater intensity of facial expression.Therefore, concluding that these facial expressionsoccurred in response to pain or were an effect ofarousal is difficult, and further study is warranted.

LimitationsWe used only one endotracheal suctioning con-

dition, had no stimulus control, and assumed thatpatients had no pain at baseline. These factors maylimit our findings in determining facial behaviorsthat may characterize the pain response. However,suctioning is comparable to other noxious proce-dures that cause pain in critically ill patients47,53; in our study, the suctioning might have had anarousal effect.

The data collection and video coding weredone by the principal investigator, who was highlyqualified and trained in FACS coding. Biasingeffects were minimized by recording the BPS scoresand coding the FACS at separate times and by cod-ing each action unit individually for all possibleaction units.

ConclusionOur findings suggest that facial expressions of

pain do not diminish in noncommunicative criti-cally ill patients. Actions in the upper part of theface (brow raiser, brow lower, and orbit tightening)are the most frequently activated expressions andmight be a valid alternative to self-report ratings in

tion in FACS coding is that the eyes are generallyopen and then close as a pain response. However,Hadjistavropoulos et al32 reported that eye closurevaried as a function of activity in patients who kepttheir eyes open to maintain balance while perform-ing physiotherapy activities. In our study, most ofthe patients had their eyes closed at onset and dur-ing the 30-second coded segment. The intensity of

eye closure was unchanged becausethis action unit is coded on basisof the degree of upper eyelid low-ering at maximum intensity wheneyes are closed for more than 2seconds. We scored patients at alevel 3 (fully tightened) on thefacial domain of the BPS if wenoted muscles around the eyescontracted as the eyelids were clos-

ing or already closed. Of note, level 3 (fully tight-ened; eg, eyelid closing) is described in FACS codingas a forced contraction of the eyelids and not justeye closure, which closely resembles action units 6and 7 and not action unit 43.25 We found no rela-tionship between eye closure (action unit 43) andlevel 3 or 4 of the facial expression component ofthe BPS. Whether eye closure or opening is associ-ated with pain or arousal warrants further studies.

Additional Facial Actions in NoncommunicativeCritically Ill Patients

Brow Raiser (Action Units 1 Plus 2). Raising ofthe inner and outer parts of the brows in responseto pain is not commonly reported in healthy volun-teers. Obviously, a poor correlation between BPSscores and descriptors not included in the BPS makessense. The facial domain of the BPS was constructedon the basis of previous findings obtained in awakevolunteers,19 a situation that would explain why browraiser was not included in the BPS descriptors.

Therefore, brow raising may havebeen an arousal effect and may notbe associated with pain response.This facial expression warrantsfurther study.

Mouth Opening (Action Units 25Plus 26). Lip parting and jaw drophave been reported in many stud-ies.26,27,30-35 Although not considereda core facial expression of pain,37

mouth opening occurred frequently in our study.Of note, most of our patients had their mouth openbecause of the presence of an endotracheal tube.However, confirming that the degree of mouthopening was due to a pain response or cough and


Facial muscleactions during pain

in the critically illwere similar to

normal volunteers.

Nose wrinkle, seenin healthy adultsduring pain, was

not strongly associ-ated with pain here.




noncommunicative critically ill patients. The FACSpain intensity scores could be used to measure painand to standardize pain evaluation. However, cau-tion must be taken in interpreting our findingsbecause we cannot state whether or not they areassociated with response to pain or are a responsedue to arousal. Further studies are needed to con-firm our findings in a larger sample with a differentlevel of sedation to account for a possible arousaleffect and during different nociceptive proceduresto determine a possible cough or respiratory distresseffect. Further studies should validate our data sothat clinicians can focus on facial expressions thatare most likely to reflect pain in noncommunicativecritically ill patients.

ACKNOWLEDGMENTSWe thank the staff, patients, and patients’ families whoparticipated in this study. We also thank the staff in theDepartment of Psychology, University of Pittsburgh, forproviding FACS training and reliability coding. Wegreatly appreciate the support in statistical analysis pro-vided by Leroy Thacker, PhD, biostatistician, Center forClinical and Translational Research, Virginia Common-wealth University.

FINANCIAL DISCLOSURESThis research was supported by grant F31 NR010433from the National Institutes of Health.

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eLettersNow that you’ve read the article, create or contribute to anonline discussion on this topic. Visit www.ajcconline.organd click “Responses” in the second column of either thefull-text or PDF view of the article.

SEE ALSOFor more about pain management in critical care, visitthe Critical Care NurseWeb site, www.ccnonline.org,and read the article by Stites, “Observational PainScales in Critically Ill Adults” (June 2013).




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SesslerMamoona Arif Rahu, Mary Jo Grap, Jeffrey F. Cohn, Cindy L. Munro, Debra E. Lyon and Curtis N.Endotracheal SuctioningFacial Expression as an Indicator of Pain in Critically Ill Intubated Adults During

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