594 Journal of Pain and Symptom Management Vol. 56 No.

4 October 2018

Brief Methodological Report

Validation of Two Pain Assessment Tools Using a

Standardized Nociceptive Stimulation in Critically Ill Adults
Cristini Klein, PhD, Wolnei Caumo, PhD, C

eline G
elinas, PhD, Val
eria Patines, RN, Tatiana Pilger, RN,
Alexandra Lopes, RN, Fabiane Neiva Backes, MD, D
ebora Feij
o Villas-Boas, PhD, and
Silvia Regina Rios Vieira, PhD
Department of Intensive Care Medicine (C.K., V.P., T.P., A.L., F.N.B., D.F.V.-B., S.R.R.V.), Clinicas Hospital from Porto Alegre (HCPA),
Porto Alegre, Brazil; Post Graduate Program in Medical Sciences (C.K., W.C., F.N.B., S.R.R.V.), Federal University of Rio Grande do Sul
(UFRGS), Porto Alegre; Laboratory of Pain & Neuromodulation (C.K., W.C.), HCPA/UFRGS, Porto Alegre; Ingram School of Nursing
(C.G.), McGill University, Montreal, Quebec, Canada; and School of Nursing (D.F.V.-B.), Federal University of Rio Grande do Sul, Porto
Alegre, Brazil

Abstract
Context. The Behavioral Pain Scale (BPS) or the Critical-Care Pain Observation Tool (CPOT) are recommended in
practice guidelines for pain assessment in critically ill adults unable to self-report. However, their use in another language
requires cultural adaptation and validation testing.
Objectives. Cross-cultural adaptation of the CPOT and BPS English versions into Brazilian Portuguese, and their validation
by comparing behavioral scores during rest, standardized nociceptive stimulation by pressure algometry (SNSPA), and turning
were completed. In addition, we explored clinical variables that could predict the CPOT and BPS scores.
Methods. A prospective cohort study was conducted with 168 medical-surgical critically ill adults unable to self-report in the
intensive care unit. Two nurses were trained to use the CPOT and BPS Brazilian Portuguese versions at the following
assessments: 1) baseline at rest, 2) after SNSPA with a pressure of 14 kgf/cm2, 3) during turning, and 4) 15 minutes after
turning.
Results. Inter-rater reliability of nurses’ CPOT and BPS scores was supported by high weighted kappa >0.7. Discriminative
validation was supported with higher CPOT and BPS scores during SNSPA or turning in comparison to baseline (P < 0.001).
The Glasgow Coma Scale score was the only variable that predicted CPOT and BPS scores with explained variance of 44.5%
and 55.2%, respectively.
Conclusion. The use of the Brazilian CPOT and BPS versions showed good reliability and validity in critically ill adults
unable to self-report. A standardized procedure, the SNSPA, was used for the first time in the validation process of these tools
and helped us improve the validation process. J Pain Symptom Manage 2018;56:594e601. Ó 2018 American Academy of Hospice
and Palliative Medicine. Published by Elsevier Inc. All rights reserved.

Key Words
Pain, critical care, pain measurement, validation study, adult, nociception

Introduction their use in another language requires cultural adapta-

tion and validation testing.
The use of the Behavioral Pain Scale (BPS) or the
This study aimed to translate the English versions
Critical-Care Pain Observation Tool (CPOT) is recom-
of the BPS and CPOT into Brazilian Portuguese, to
mended in practice guidelines for pain assessment in
validate their use in Brazilian adult intensive care
critically ill adults unable to self-report.1 However,
unit (ICU) settings and to identify demographic

Address correspondence to: Cristini Klein, PhD, Dom Pedro I, Accepted for publication: June 25, 2018.
50. Ivoti, RS 93900-000, Brazil. E-mail: ckklein@hcpa.edu.br

Ó 2018 American Academy of Hospice and Palliative Medicine. 0885-3924/$ - see front matter
Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jpainsymman.2018.06.014
Vol. 56 No. 4 October 2018 Pain Tool Validation With Standardized Stimulation
and clinical variables that influenced the CPOT and
BPS scores. In previous validation studies of the BPS
and CPOT, standard of care procedures performed
in the ICU, such as turning, endotracheal suction,
mobilization, and others as nociceptive stimuli,2e10
were mainly used. These care procedures are not
standardized, are performed by different clinicians,
and may influence the patients’ behavioral re-
sponses. For the first time in this study, a standard-
ized nociception stimulation called the pain
algometry pressure test was also used11e14 to
enhance the validation process, that is, using the
strategy of discriminative validation between painful
and nonpainful conditions.
Methods
This prospective cohort study was conducted in a
medical-surgical ICU from a University Hospital in the
South of Brazil. From April to December 2014, research
staff screened all patients for eligibility on weekdays
from 8.00 AM to 2.00 PM. Patients older than eight years,
unable to self-report verbally, conscious or unconscious
were included. Patients with no physical response to a
painful stimulus, that is, those who were quadriplegic,
received neuromuscular blocking agents, or had a
Fig. 1. Flow of the translation and cultural adaptation. CPOT ¼ Critical-Care Pain Observation Tool; BPS ¼ Behavioral Pain
Scale; ICU ¼ intensive care unit.
595
Glasgow Coma Scale (GCS) score of less than four on
the item motor response15 were excluded. Also, pa-
tients receiving continuous intravenous (IV) infusions
of analgesic or sedative agents, with an injury to the
face or both upper limbs, were excluded.
CPOT and BPS
Both the CPOT3 and BPS3,4 were developed to
assess pain in ICU patients unable to self-report. The
CPOT consists of four behavioral items: 1) facial ex-
pressions, 2) body movements, 3) compliance with
the ventilator (intubated patients) or vocalization
(nonintubated patients), and 4) muscle tension.
Each behavioral item is scored on a scale from 0 to
2. BPS is composed of three behavioral items: 1) facial
expression, 2) movements of upper limbs, and 3)
compliance with the ventilator. Each behavioral item
is scored on a scale from 1 to 4.
Translation and Cultural Adaption
The translation into Brazilian Portuguese and cross-
cultural adaptation of the original English versions of
the CPOT2 and BPS3,4 was performed based on estab-
lished guidelines.16 The recommended steps were per-
formed and included the translation, translation
596 Klein et al.
synthesis, back translation, expert committee, and pi-
lot testing (Fig. 1).
Validation
The validation testing was performed in ICU pa-
tients when exposed to two procedures: 1) standard-
ized nociceptive stimulation by pressure algometry
(SNSPA) and 2) standard care (turning). The valida-
tion study phases are presented in Fig. 2 and included
seven assessments.
Algometry pressure test (threshold and tolerance)
is a validated quantitative method used in the field
of pain (activates mechanosensitive nociceptors in
the skin).11e14 It consists of a handheld pressure algo-
meter (Somedic AB, Stockholm, Sweden) with a rub-
ber probe with a surface area of 1 cm2 that was
applied perpendicularly to the skin by the principal
researcher, on the lateral proximal tibia surface, on
the dominant site of the body. Algometer was used
to measure pressure pain threshold (PPT) and
SNSPA.
PPT instances 1e3 were considered to be the mini-
mal pressure necessary to trigger one of the pain be-
haviors as assessed by the CPOT or BPS. The median
PPT was established by three sequences of the test
(limit 1e3).12 PPT is important to measure to deter-
mine the minimal pressure necessary to evoke hierar-
chical pain behavior. Considering the safety of the
patient and based on previous studies, we standard-
ized a maximum pain stimulus of 14 kgf/cm2 for all
patients, and we referred to it as SNSPA.13,14
Research staff described demographic data with the
patient’s legal guardian and using the electronic patient
record. Opioids (methadone, codeine, and fentanyl)
used in the previous 24 hours before data collection
were converted into an equivalent dose of morphine
(milligrams) divided by the patient’s weight in kilogram.
Statistical Analysis
Absolute values and percentages were obtained for
categorical variables; and means (SD) or medians
(25the75th percentiles) were calculated for
Fig. 2. Flow of pain assessments.
Vol. 56 No. 4 October 2018
continuous variables according to data distribution
(Shapiro-Wilk test #0.05). To analyze the distribution
of the CPOT and BPS scores, we calculated the ceiling
effect (patients with the highest possible score) and
floor effect (patients with the lowest possible score).
Inter-rater reliability was estimated by weighted kappa
coefficients (95% CI) at each assessment between the
two rater’s scores. To assess reliability, we measured
homogeneity through mean interitem correlation. In-
teritem correlations mean a range between 0.20 and
0.40 is expected to be a good reliability.17 For discrim-
inative validation, we used the Friedman test with
Dunn post hoc tests. Effect size estimated by the Ken-
dall’s W test assumes reference value 0 (no relation-
ship) to 1 (perfect relationship).18 We selected
relevant demographic and clinical variables and per-
formed Spearman analysis (rho). After the binary
analysis, considering P # 0.05, we found an associa-
tion between the CPOT or BPS scores and the GCS
scores, age, and the number of analgesics adminis-
tered within the previous 24 hours before the assess-
ment. We used a linear regression model and
included variables with significant correlation in a bi-
nary analysis simultaneously (enter method) to pre-
dict CPOT and BPS scores during SNSPA. We
verified assumptions such as normality of residuals,
homoscedasticity, autoregression, and multicollinear-
ity. A P-value of #0.05 was considered statistically sig-
nificant for all tests.
Analyses were performed using the Statistical
Package for Social Sciences, version 18.0 (SPSS Inc,
Chicago, IL). The sample size was based on the pri-
mary objective related to discriminative validation.
The sample size was calculated in WinPepi program,
version 11.48, based on SD from pretesting with 30
ICU patients.19 Considering that results at baseline
and 15 minutes after SNSPA were not different, we
found score from the scale difference to be detected
from 0.5 significant level, power 90%, SD .6e1.7,
and correlation coefficient from 0.1 between rest
and SNSPA on the CPOT or BPS tool. The minimal
sample size required was 163.
Vol. 56 No. 4 October 2018 Pain Tool Validation With Standardized Stimulation 597

Results
A total of 1019 ICU patients were screened, 844
excluded, 175 patients included for assessment, seven
excluded during protocol because they required
continuous IV infusion of analgesic or sedative agents,
and 168 of them were included in data analysis (see
screening flowdFig. 3). Algometry pressure tests
were performed in all 168 patients, and turning was
done only in 124 patients because of patient’s insta-
bility and other reasons.
Demographic and clinical characteristics of patients
included in the study are described in Table 1. A total
of 1132 paired assessments were performed. Only 30
(17.9%) of the patients did not receive analgesia
within the previous 24 hours before data collection,
78 (46.4%) received only one analgesic dose, and 60
(35.7%) more than two analgesic doses. Most of
them (69 [41%]) received fentanyl IV.
Distribution of the CPOT and BPS Scores
Descriptive results of CPOT and BPS scores after
SNSPA and after turning are shown in Table 2, respec-
tively. The CPOT and BPS scores ranged from the mini-
mum to maximum for all items after SNSPA and turning.
The maximal ceiling effect after SNSPA of CPOT
and BPS was vocalization, with 65.2% and 60.9%,
respectively. Considering that most patients were me-
chanically ventilated (84.5%), vocalization was not
applicable to these patients. Facial expression was
the other more pronounced pain behavior, with
ceiling effect of 61.9% for CPOT and 58.3% for BPS,
after SNSPA (Table 2). The floor effect, showing the
lowest score possible, was found for facial expression
with 3% and 3.6% after SNSPA for both scales
(Table 2).
The maximal ceiling effect after turning was attrib-
uted to compliance with the ventilator for the CPOT
and vocalization for the BPS, with 52.7 and 34.8%,
respectively. The floor effect was found for compliance
by the ventilator for both scales after turning with 1%
and 2%, respectively (Table 2).
A variation occurred for vocalization as it was influ-
enced by its applicability to the patient’s condition.
The vocalization item showed the higher ceiling ef-
fects during SNSPA but was not as high during
turning. The skewness test showed that most of the
items of both scales had symmetric distribution, with
a deviation to the left of the vocalization item in
both scales. The kurtosis values showed normal distri-
bution of all items of both scales.
Reliability
The mean interitem correlation (homogeneity) to
SNSPA for CPOT was 0.35 (range 0.24) and BPS 0.34
(range 0.1) and for mechanically ventilated patients
and nonventilated patients 0.39 (range 0.57) and
0.44 (range 0.16), respectively.
Inter-rater reliability of CPOT and BPS scores was
performed at the four assessments and supported
with high weighted kappa coefficients >0.8 between

Patients Screened: 1019

Excluded: 844
Communicative Patient 335
Analgesic or Sedation use 238
GCS <4 (item motor response) 84
Neurodegenerative Disease 48
Increased Bleeding Propensity 32
Quadriplegic 30
Palliative Care 26
Injury on Face or Upper Limb 23
Investigated Brain Dead 16
Without Consent 12
Patients Included for Assessment: 175

Excluded Re-sedation: 7

Patients Included for Assessment:168

Fig. 3. Diagram of screening. GCS ¼ Glasgow Coma Scale.

598 Klein et al. Vol. 56 No. 4 October 2018

Table 1 (39.2%), and compliance with ventilator (24.5%)

Main Demographic and Clinical Characteristics of were reached.
Patients Included in the Study (N ¼ 168)
Characteristics N %
Discriminative Validation
Age (yrs)a
65  15 Discriminative validation was supported by higher
Gender, male 88 52.4
APACHE IIa 24  8
median CPOT and BPS scores during SNSPA and
BMI (kg/m2)b 27 (23e32) turning in comparison to baseline at rest and 15 mi-
ICU stay before data collection (days)a 5.68 (6.06) nutes after turning. Differences were found between
GCSa 9.7 (1.6)
Abdominal disease 38 22.6
CPOT scores (median and interquartile range
Cardiovascular disease 33 19.6 [25the75th percentile]) at baseline (0, 0e0), SNSPA
Brain injury 32 19 (5, 4e7) (c2 ¼ 317; degrees of freedom [df] ¼ 2; Ken-
Others 20 11.9
Patients who required surgery 35 20.8
dall’s W ¼ 0.94; P < 0.05), turning (5, 3e6.75)
Mechanical ventilation use 142 84.5 (c2 ¼ 232; df ¼ 2; Kendall’s W ¼ 0.93; P < 0.05),
Medication regimen and 15’ after turning (0, 0e0) (P < 0.05). Differences
Sedationc 44 25.9
Analgesiad 138 81.2
were also found between BPS scores at rest (3, 3e3),
Number of analgesice SNSPA (8, 7e10) (c2 ¼ 319; df ¼ 2; Kendall’s
1 analgesic 78 45.9 W ¼ 0.98; P < 0.05), turning (8, 6e9.759)
$2 analgesics 60 35.3
Comorbidities 159 94.6
(c2 ¼ 230; df ¼ 2; Kendall’s W ¼ 0.92; P < 0.05),
Hypertension 102 60.7 and 15’ after turning (3, 3e3) (P < 0.05). We did
Diabetes mellitus 50 29.8 not find differences between CPOT and BPS scores
Chronic renal failure 37 22
Stroke 35 20.8
during both procedures.
Cancer 31 18.5
Dose received within previous 24 hoursb Predictive Validation of CPOT and BPS Scores
Equianalgesic morphine (mg/24 hours/kg) 0 (0e0.91)
Midazolam (mg/24 hours/kg) 0 (0e0.11) A linear regression model including variables of
APACHE ¼ Acute Physiology and Chronic Health Evaluatio II; BMI ¼ body
age, GCS, type of analgesics and doses administered
mass index; ICU ¼ intensive care unit; GCS ¼ Glasgow Coma Scale. within 24 hours before data collection was used to pre-
a
Mean  SD.
b
Median interquartile range: 25the75th percentile.
dict CPOT and BPS scores during SNSPA. The GCS
c
Medication regimen, the number of analgesic doses administered within score was the only variable that predicted CPOT and
24 hours before data collection: We compiled sedation, independent by the
route of administration.
BPS scores. A significant regression equation was
d
Medication regimen, the number of analgesic doses administered within found: F ¼ 17.93 (df1 ¼ 3, df2 ¼ 163, P < 0.001)
24 hours before data collection: We compiled analgesic intermittent doses
administered within the previous 24 hours, independent by the route of
with an R2 of 0.24 and an adjusted R2 of 0.23. CPOT
administration. score increased half a point (0.44) for each point in
e
Number of doses of any analgesic, independent by the route of
administration.
GCS (95% CI 0.35e0.65). And to BPS was found
F ¼ 22.64 (df1 ¼ 3, df2 ¼ 163, P < 0.001), R2 of
0.29, and an adjusted R2 of 0.28. BPS score increased
the two trained nurse raters. During SNSPA, weighted half a point (0.44) for each point in GCS (95% CI
kappa coefficients (95% CI) of CPOT and BPS scores 0.52e0.87).
were 0.96 (0.95e0.97) and 0.96 (0.94e0.97)
(P < 0.001), respectively. During turning, weighted
kappa coefficients (95% CI) of CPOT and BPS scores
were 0.96 (0.94e0.97) and 0.94 (0.92e0.95) Discussion
(P < 0.001), respectively. The Brazilian versions of the CPOT and BPS showed
good reliability (homogeneity and validity) in ICU pa-
tients unable to self-report. To our knowledge and for
the first time in this validation study, a standardized
Pain Pressure Threshold nociceptive stimulation (i.e., SNSPA) was used.
The median pressure threshold was 5 kgf/cm2 (in- Discriminative validation of both Brazilian scale ver-
terquartile range 1e5 kgf/cm2). The minimal pres- sions was supported by higher CPOT and BPS scores
sure required to induce the first pain response was during SNSPA and turning when compared with rest
assessed with the CPOT and BPS. More specifically at baseline and after turning. In addition to SNSPA,
for the CPOT, higher scores of body movements turning that is a routine care procedure was used in
(78.9%), facial expressions (54.2%), muscle tension the present study similarly to previous CPOT and
(41.5%), vocalization (39.15), and compliance by the BPS validation studies.20e22 Although the behavioral
ventilator (30%) were reached. According to the responses during turning are accessible and easy to
BPS, higher scores of movements of upper limbs observe, and it is a suitable method for this setting,
(56.6%), facial expression (53.6%), vocalization it is also known that such stimulation can evoke
Vol. 56 No. 4 October 2018 Pain Tool Validation With Standardized Stimulation 599

Table 2
Effects After SNSPA and Turning
Scale Mean (SD) Median (Range) Ceiling Effect (%) Floor Effect (%) Skewness Kurtosis

After SNSPA (N ¼ 168)

CPOT
Facial expression 1.59 (.55) 2 (1e2) 61.9 3 0.90 0.22
Body movements 1.4 (.57) 1 (1e2) 44.6 4.2 0.30 0.78
Compliance with ventilator 1 (.56) 1 (1e1) 15.9 15.9 0 0.2
Vocalization 1.57 (.66) 2 (1e2) 65.2 8.7 1.28 0.62
Muscle tension 1.28 (.71) 1 (1e2) 43.5 15.5 0.47 0.94
BPS
Facial expression 3.32 (.9) 4 (3e4) 58.3 3.6 0.97 0.33
Movements of upper limbs 2.7 (1.01) 3 (2e4) 25.6 15.5 0.27 1.02
Compliance with ventilator 1.96 (.62) 2 (2e2) 1.4 20 0.37 0.87
Vocalization 3.3 (1.02) 4 (3e4) 60.9 8.7 1.24 0.32
After turning (N ¼ 124)
CPOT
Facial expression 0.98 (.75) 1 (0e2) 27.4 29.8 0.04 1.25
Body movements 1.11 (.74) 1 (1e2) 33.3 22.8 0.17 1.16
Compliance with ventilator 1.51 (.52) 2 (1e2) 52.5 1 0.27 1.44
Vocalization 0.87 (.69) 1 (0e1) 17.4 30.4 0.17 0.75
Muscle tension 1.17 (.77) 1 (1e2) 39.5 22.6 0.30 1.26
BPS
Facial expression 2.46 (1.16) 2 (1e4) 26.6 28.2 0.06 1.45
Movements of upper limbs 2.59 (1.08) 3 (2e3.75) 25 21 0.13 1.24
Compliance with ventilator 2.53 (.64) 2 (2e3) 5.9 2 0.33 0.27
Vocalization 2.57 (1.23) 2 (1e4) 34.8 26.1 0.00 1.65
SNSPA ¼ standardized nociceptive stimulation by pressure algometry; CPOT ¼ Critical-Care Pain Observation Tool; BPS ¼ Behavioral Pain Scale.
Interquartile range: 25the75th percentile.

many other reactions besides pain such as general
discomfort, distress, and coughing, among others.23,24
Thus, the use of a standardized and an enshrined
approach to measure pain threshold enhanced the
validation process of the CPOT and BPS. In fact, the
SNSPA allowed us to standardize the intensity of
the painful stimulation applied to ICU patients11
because the SNSPA is known to5: 1) activate the noci-
ceptive pathways (mechanoreceptor fibers a and
delta), 2) reduce possible bias to evoke the pain
response, 3) improve the validation process of the psy-
chometric properties of the CPOT and BPS for the
assessment of pain in patients unable to self-report,
and 4) offer an interesting option to facilitate compar-
isons of findings across studies and reproducibility be-
tween studies. In both scales, facial expressions were
the most consistent behaviors related to pain, which
is consistent with previous studies.21,25,26 In fact, the
facial expression item displayed lower rates of the
floor effect during SNSPA in both scales. Facial expres-
sion scores were lower during turning compared with
SNSPA. Thus, different approaches to induce nocicep-
tive stimulation, which also has the capacity to induce
behavioral responses, may be used as complementary
methods in the validation process. This behavior prob-
ably occurred because each stimulation distinctly acti-
vates pain pathways.
Compliance with the ventilator showed low scores
after SNSPA (Table 2). On the opposite, higher
scores on compliance with the ventilator were
observed during turning. A possible explanation
for this result is that compliance with the ventilator
was altered with movements involved during turning,
which is not specific to pain and could be modified
by secretion mobilization or patient awakening.27,28
Hence, turning caused coughing; which is included
in both scales.
Vocalization was not assessable in all ICU patients.
The vocalization item showed the higher ceiling ef-
fects and deviation to the left in both scales during
SNSPA, whereas this criterion was not so pronounced
during turning (Table 2). According to Chanques
et al.,4 vocalization included in the BPS-
nonintubated led to better psychometric properties,
probably because it is easier to identify the behavior
compliance with ventilator, which showed lower perfor-
mance in identifying response associated with pain.
According to the body movements and muscle ten-
sion items in the CPOT and movements of upper
limbs in the BPS, we found median ceiling effects
(Table 2). Considering that many factors may alter
behavioral responses in ICU patients (e.g., polyneur-
opathy, physical restraints, analgesic agents),29e31
this could have influenced body movements and
pain behaviors exhibited by patients in this study.
However, these results suggest a possible interference
by other factors, such as immobilization, disease, anal-
gesic or sedative medication, and others.
An additional analysis was made to predict CPOT
and BPS scores, and it was found that the GCS score
was a significant predictor. More specifically, the high-
er the GCS score was, the higher the CPOT and BPS
600 Klein et al.
scores were during SNSPA. This finding is consistent
with previous studies in which pain behaviors were
likely to be exhibited by conscious patients compared
with those unconscious.3,32e34 Such finding may sug-
gest that specific cut points could be established ac-
cording to the patient’s level of consciousness.
The present study has some limitations. First, only
research nurses evaluated the two scales, and bedside
nurses were not involved, which could have increased
the kappa coefficient values. Second, the use of the
scales was not performed in a random sequence; the
CPOT was completed first and the BPS second.
In conclusion, the study findings supported the reli-
ability and validity of the use of the Brazilian Portu-
guese versions of the CPOT and BPS for the
assessment of pain in ICU patients unable to self-
report, and this was demonstrated with both a routine
care procedure (turning) and an SNSPA. SNSPA
helped us improve the validation process of both
scales, and we suggest the use of standardized proced-
ure in the next studies to improve the ability to gener-
alize and reduce possible bias to evoke the pain
response in this vulnerable group.
Disclosures and Acknowledgments
This study was supported by the Hospital de Clinicas
de Porto Alegre (Postgraduate Research Group -
FIPE) institution that received support from govern-
mental Brazilian agencies. The authors thank Stepha-
nie Lopresti for her linguistic assistance. They also
thank the contributions of Luciano Santos Pinto
Guimar~aes for statistical advice. The authors declare
no conflicts of interest.
Ethical approval: The Human Research Committee
of the Health Center of the Clinicas Hospital from
Porto Alegre, Brazil, approved this study by the num-
ber 12e0395 and 12e0443, according to the Declara-
tion of Helsinki (Resolution Health 466/12 of
National Health Council). Written informed consent
was obtained from the patients’ legal representatives
who agreed to participate in this study.
References
1. Barr J, Fraser GL, Puntillo K, et al. Clinical practice
guidelines for the management of pain, agitation, and
delirium in adult patients in the intensive care unit. Crit
Care Med 2013;41:263e306.
2. G
elinas C, Fillion L, Puntillo KA, Viens C, Fortier M.
Validation of the critical-care pain observation tool in adult
patients. Am J Crit Care 2006;5:420e427.
3. Payen JF, Bru O, Bosson JL, et al. Assessing pain in crit-
ically ill sedated patients by using a behavioral pain scale.
Crit Care Med 2001;29:2258e2263.
Vol. 56 No. 4 October 2018
4. Chanques G, Payen JF, Mercier G, et al. Assessing pain in
non-intubated critically ill patients unable to self report: an
adaptation of the Behavioral Pain Scale. Intensive Care Med
2009;35:2060e2067.
5. Hsiung NH, Yang Y, Lee MS, Dalal K, Smith GD. Trans-
lation, adaptation, and validation of the behavioral pain
scale and the critical-care pain observational tools in Taiwan.
J Pain Res 2016;15:661e669.
6. Hyl

en M, Akerman E, Alm-Roijer C, Idvall E. Behavioral
Pain Scaledtranslation, reliability, and validity in a Swedish
context. Acta Anaesthesiol Scand 2016;60:821e828.
7. Chen J, Lu Q, Wu XY, et al. Reliability and validity of the
Chinese version of the behavioral pain scale in intubated
and non-intubated critically ill patients: two cross-sectional
studies. Int J Nurs Stud 2016;61:63e71.
8. A€ıssaoui Y, Zeggwagh AA, Zekraoui A, Abidi K,
Abouqal R. Validation of a behavioral pain scale in critically
ill, sedated, and mechanically ventilated patients. Anesth An-
alg 2005;101:1470e1476.
9. Rafiei M, Ghadami A, Irajpour A, Feizi A. Validation of
critical care pain observation tool in patients hospitalized
in surgical wards. Iran J Nurs Midwifery Res 2016;21:
464e469.
10. Sulla F, De Souza Ramos N, Terzi N, et al. Validation of
the Italian version of the Critical Pain Observation Tool in
brain-injured critically ill adults. Acta Biomed 2017;88:
48e54.
11. Staahl C, Drewes AM. Experimental human pain
models: a review of standardised methods for preclinical
testing of analgesics. Basic Clin Pharmacol Toxicol 2004;
95:97e111.
12. Finocchietti S, Andresen T, Arendt-Nielsen L, Graven-
Nielsen T. Pain evoked by pressure stimulation on the tibia
bonedinfluence of probe diameter on tissue stress and
strain. Eur J Pain 2012;16:534e542.
13. Fischer AA. Pressure tolerance over muscles and bones
in normal subjects. Arch Phys Med Rehabil 1986;67:
406e409.
14. Andersen H, Arendt-Nielsen L, Danneskiold-Samsøe B,
Graven-Nielsen T. Pressure pain sensitivity and hardness
along human normal and sensitized muscle. Somatosens
Mot Res 2006;23:97e109.
15. Nassar Junior AP, Pires Neto RC, de Figueiredo WB,
Park M. Validity, reliability and applicability of Portuguese
versions of sedation-agitation scales among critically ill pa-
tients. Sao Paulo Med J 2008;126:215e219.
16. Beaton DE, Bombardier C, Guillemin F, Ferraz MB.
Guidelines for the process of cross-cultural adaptation of
self-report measures. Spine 2000;25:3186e3191.
17. Clark LA, Watson D. Constructing validity: basic issues in
objective scale development. Psychol Assess 1995;7:309e319.
18. Tomczak M, Tomczak E. The need to report effect size
estimates revisited. An overview of some recommended mea-
sures of effect size. Trends Sport Sci 2014;1:19e25.
19. Abramson JH. WINPEPI (PEPI-for-Windows): computer
programs for epidemiologists. Epidemiol Perspect Innov
2004;17:6.
20. Li Q, Wan X, Gu C, et al. Pain assessment using the
critical-care pain observation tool in Chinese critically ill
ventilated adults. J Pain Symptom Manage 2014;48:975e982.
Vol. 56 No. 4 October 2018 Pain Tool Validation With Standardized Stimulation
21. G
elinas C, Puntillo KA, Joffe AM, Barr J. A validated
approach to evaluating psychometric properties of pain
assessment tools for use in nonverbal critically ill adults.
Semin Respir Crit Care Med 2013;34:153e168.
22. Chanques G, Pohlman A, Kress JP, et al. Psychometric
comparison of three behavioural scales for the assessment
of pain in critically ill patients unable to self-report. Crit
Care 2014;18:R160.
23. G
elinas C, Chanques G, Puntillo K. In pursuit of pain:
recent advances and future directions in pain assessment
in the ICU. Intensive Care Med 2014;40:1009e1014.
24. Puntillo KA, White C, Morris AB, et al. Patients’ percep-
tions and responses to procedural pain: results from Thun-
der Project II. Am J Crit Care 2011;10:238e251.
25. G
elinas C, Harel F, Fillion L, Puntillo KA, Johnston CC.
Sensitivity and specificity of the critical-care pain observation
tool for the detection of pain in intubated adults after car-
diac surgery. J Pain Symptom Manage 2009;37:58e67.
26. Arif-Rahu M, Grap MJ. Facial expression and pain in the
critically ill non-communicative patient: state of science re-
view. Intensive Crit Care Nurs 2010;26:343e352.
27. Gracely RH, Undem BJ, Banzett RB. Cough, pain and
dyspnoea: similarities and differences. Pulm Pharmacol
Ther 2007;20:433e437.
601
28. Hewitt N, Bucknall T, Faraone NM. Lateral positioning
for critically ill adult patients. Cochrane Database Syst Rev
2016;12:CD007205.
29. Hermans G, Van den Berghe G. Clinical review: inten-
sive care unit acquired weakness. Crit Care 2015;19:274.
30. Witteveen E, Wieske L, Verhamme C, et al. Muscle and
nerve inflammation in intensive care unit-acquired weak-
ness: a systematic translational review. J Neurol Sci 2014;
345:15e25.
31. Borges RC, Carvalho CR, Colombo AS, da Silva
Borges MP, Soriano FG. Physical activity, muscle strength,
and exercise capacity 3 months after severe sepsis and septic
shock. Intensive Care Med 2015;41:1433e1444.
32. Cameron S, Ball I, Cepinskas G, et al. Early mobilization
in the critical care unit: a review of adult and pediatric liter-
ature. J Crit Care 2015;30:664e672.
33. G
elinas C, Arbour C. Behavioral and physiologic indica-
tors during a nociceptive procedure in conscious and uncon-
scious mechanically ventilated adults: similar or different?
J Crit Care 2009;24:628.e7-17.
34. Ahlers SJ, van der Veen AM, van Dijk M, Tibboel D,
Knibbe CA. The use of the Behavioral Pain Scale to assess
pain in conscious sedated patients. Anesth Analg 2010;110:
127e133.