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REVIEW
KEYWORDS
Pain;
Pain assessment;
Behaviours;
Vital signs;
Pupillometry;
Critically ill;
Intensive care
Summary Pain assessment in the critically ill adult remains a daily clinical challenge. Position statements and practice guidelines exist to guide the ICU care team in the pain assessment
process. The patients self-report of pain remains the gold standard measure for pain and
should be obtained as often as possible. When self-report is impossible to obtain, observational
pain scales including the Behavioural Pain Scale (BPS) and the Critical-Care Pain Observation
Tool (CPOT) have been recommended for clinical use in the critically ill adult. However, their
adaptation and validation in brain-injured and burn ICU patients is required. Family caregivers
may help in the identication of pain-related behaviours and should be more involved in the
ICU pain assessment process. Fluctuations in vital signs should only be considered as cues for
further assessment of pain with appropriate tools, and may better represent adverse events of
severe pain. Other physiologic measures of pain should be explored in the ICU, and pupillometry
appears as a promising technique to further study. Implementation of systematic pain assessment approaches using tools adapted to the patients ability to communicate and condition
has shown positive effects on ICU pain practices and patient outcomes, but randomised control
trials are needed to conrm these conclusions.
2016 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.iccn.2016.03.001
0964-3397/ 2016 Elsevier Ltd. All rights reserved.
Introduction
Pain is an enduring concern and a common symptom in
critically ill adults. Indeed, pain has been shown to be experienced at rest by more than 30% of patients (Chanques
et al., 2007), and this percentage exceeds 50% during
common care procedures in the intensive care unit (ICU)
(Glinas, 2007a; Puntillo et al., 2001, 2014). Turning, endotracheal suctioning, tube or drain removal, wound care
and arterial line insertion are procedures described as the
most painful by ICU patients in large international studies
(Puntillo et al., 2001, 2014). Nurses are facing numerous
challenges with pain assessment in the ICU as many patients
are unable to self-report because of various factors such as
altered level of consciousness (LOC), sedation and mechanical ventilation. Under-assessment of pain represents one
of the primary barriers to the adequate treatment of pain
in critically ill patients (Pasero et al., 2009). The evidence
demonstrating absent or incomplete assessment of pain is
associated with negative patient outcomes such as longer
duration of mechanical ventilation and ICU length of stay,
and increased mortality (Kastrup et al., 2009; Payen et al.,
2009), is a particular concern for nurses. This paper might
help nurses in reversing this situation through the review of
steps for proper pain assessment, recent evidence and new
trends in measures and indicators for the assessment of pain
in the critically ill adult.
C. Glinas
family or caregiver about the patients pain behaviours; and
(4) attempt an analgesic trial when pain is suspected, and
reassess for pain (Herr et al., 2011).
The 010 Numeric Rating Scale (NRS) is commonly used
in clinical practice, and an enlarged visual format of the
NRS was found to be the most feasible and discriminative
self-report scale in comparison to other scales (i.e., visual
analogue scale, verbal descriptor scale) and formats (i.e.,
oral versus visual) for measuring pain intensity in critically
ill adult patients (Chanques et al., 2010). The vertical thermometer format has also been found to be easier to use by
critically ill adults and older adults (Glinas, 2007b; Herr,
2011). When a self-report of pain intensity is not possible,
a simple yes or no indicating the presence versus the
absence of pain should be considered as a valid self-report
(Herr et al., 2011). When self-report of pain is impossible
to obtain, validated behavioural pain scales should be used
as alternative measures for pain assessment. The family can
also provide the care team with relevant information on the
patients pain behaviours to enhance the detection of pain.
However, not much is known about the family members
perception of patients pain-related behaviours in the ICU
context. To our knowledge, only one qualitative study has
been conducted with seven family members of ICU patients
with a traumatic brain injury (TBI) (Vanderbyl and Glinas,
2014). Interestingly, family members identied behaviours
indicative of pain similar to those included in most scales
recommended for clinical use such as facial expressions,
body movements and muscle rigidity. More specically, they
described movements of the eyes and the mouth, tears or
eye weeping, touching or trying to touch the pain site and
visible muscle tension. They also provided meaningful explanations of their perception in relation to their knowledge
of the patient. Another study examined the interrater reliability of proxy reporters of pain (Puntillo et al., 2012).
Family proxy reporters were found to be closer to ICU
patients self-reports when compared to nurses and physicians. Specically in regards to pain, moderate intraclass
correlation coefcient (ICC) of 0.43 and 0.45 were found
between patient-family member reports of pain intensity
and pain distress, respectively. Lower ICCs of 0.190.40
were obtained between patient-nurse and patient-physician
pain reports (Puntillo et al., 2012). Unfortunately, little evidence exists about proxy reporters reliability in the pain
assessment process and further research is necessary.
The Communication Model of Pain (Hadjistavropoulos and
Craig, 2002; Hadjistavropoulos et al., 2011) also offers an
interesting conceptual foundation for the assessment of pain
(Fig. 1). This A B C model conceptualises pain as an internal state (A) that may be encoded in particular features of
expressive behaviours (B), allowing observers or raters to
draw inferences (C) about the nature of the patients experience. More specically, the processing of the pain stimulus
is modulated by intrapersonal and/or contextual factors (A)
inuencing the way pain is experienced in each individual.
Gender, age, ethnicity, health condition and the context in
which this individual is evolving are examples of these factors. The use of mechanical ventilation and the administration of analgesic and sedative agents are more specic to the
critical care context and add challenges to pain assessment.
The pain stimulus is encoded in self-report (for patients able
to communicate) and behaviours (B) which are decoded by
Figure 1
Adapted from the Communication Model of Pain (Hadjistavropoulos and Craig, 2002).
observers (C). Self-report depends on higher mental processing while behaviours are less subject to voluntary control
and are more automatic. Behaviours may be more difcult
to decode by observers, and educational training is of great
importance to support them in developing the competence
of adequately assessing pain behaviours using observational
measures. For example, standardised training for the use
of BPS and CPOT has led to appropriate tool utilisation into
practice and consistent scoring among ICU nurses and physicians (Chanques et al., 2006; Glinas et al., 2011a,b).
Such a conceptual framework may guide nurses in considering different aspects of the patients situation and the
context in which he/she is evolving in the pain assessment
process. It also provides a strong scientic basis for the
most appropriate methods to assess pain i.e., self-report and
behavioural observation to be interpreted by decoders (e.g.,
nurses and family caregivers). Furthermore, it ts nicely
with the current recommendations and guidelines for pain
assessment (Barr et al., 2013; Herr et al., 2011).
Cut-off scores for the presence of pain have been established for the BPS (>5) (Payen et al., 2007) and CPOT (>2)
(Glinas et al., 2009) which both represent more than two
points from their respective minimal score. Behavioural pain
scores based on the nurses observation of the patient should
be interpreted differently from the patients self-report pain
intensity scores. In fact, although they both represent pain
scores, they are not measuring the same dimension of pain.
More specically, the patients self-report of pain intensity
relates to the sensory dimension of pain which refers to
the perception of pain by the person who is experiencing
it (Melzack and Casey, 1968). On the other hand, the nurses
observational scores are associated with the behavioural
component of pain i.e., behavioural responses exhibited by
patients to express their pain (McGuire, 1992) and decoded
by an external observer (as illustrated in the C component of
Fig. 1). Self-reported pain intensity scores and behavioural
Figure 2
C. Glinas
Pain Intervention Algorithm Glinas C (2016). NRS, Numeric Rating Scale; CPOT, Critical-Care Pain Observation Tool.
pain scores move in the same direction (i.e., when one score
increases, the other score increases as well) (Herr et al.,
2011; Glinas et al., 2013), but are not equal scores. Moreover, while it is useful to classify the intensity of pain as mild,
moderate and severe for the development of pain management protocols, it is important to know that behavioural
pain scales only allow the detection of the presence versus
absence of pain. Indeed, in most studies, this criterion of
presence versus absence of pain was used to establish BPS
(Chen et al., 2014) and CPOT (Echegaray-Benites et al.,
2014; Glinas and Johnston, 2007; Li et al., 2014) cut-off
scores. However, in a previous study with postoperative
ICU patients, it was found that the CPOT cut-off score >2
could better classify patients who self-reported moderate
to severe pain (Glinas et al., 2009). Knowing this, opioid and/or non-opioid analgesic agents could be trialled
when cut-off scores of behavioural pain scales are reached.
An intervention algorithm with the CPOT was created to
help guide the ICU care team in their decision for pain
management (Fig. 2), and its implementation still needs to
be trialled in clinical practice. Nevertheless, pain management protocols must be adapted to take into account that
behavioural pain scores cannot discriminate between mild,
moderate and severe levels of pain.
5
(median = 0; range 06) (p < 0.001). Patients who reported
pain during turning had higher CPOT scores than those
who reported no pain (p < 0.001), and a moderate positive
correlation was obtained with their 010 NRS self-report
(rs = 0.57; p < 0.001). A CPOT cut-off score 2 showed sensitivity and specicity ndings of 76.9% and 73.3% respectively
and the ability to discriminate (Area Under the Curve or AUC)
between those with or without pain was high at 86.4%.
Only one American study was conducted in a burn population (Wibbenmeyer et al., 2011) and evaluated two pain
scales including the CPOT (Glinas et al., 2006) and the NonVerbal Pain Scale (NVPS: Odhner et al., 2003). The NVPS
includes three behavioural items (i.e., facial expression,
activity and muscle guarding) and two physiologic ones in
relation to changes in vital signs (i.e., blood pressure and
heart rate) and others (i.e., skin temperature, diaphoresis,
dilated pupils and ushing) for a possible total score ranging
from 0 to 10 (Odhner et al., 2003). A total of 225 paired
assessments were performed in 38 burn patients at rest,
before and after daily activities (either wound cleansing or
physical/occupational therapy). Flame or ash burn was the
most common aetiology (76.3%) and the average burn size
was 10.4% (SD = 12.1%) of body surface area. CPOT and NVPS
scores were shown to discriminate between pain at rest and
during activity but remained low with mean scores <1. In this
sample, patients were able to self-report and mild positive
correlations were obtained between behavioural scores and
the 010 NRS scores with Pearson coefcients of 0.36 (for
CPOT) and 0.38 (for NVPS) (p < 0.01). It is worth mentioning
that means of 4.27 and 5.41 of self-reported 010 NRS scores
were described at rest and during activity respectively showing moderate perceived pain in this sample. Again, the item
scores were not presented making it impossible to identify the behavioural responses exhibited by these patients.
Moreover, the body area was not specied which would have
been useful in better understanding the pain scores. For
example, we could expect that patients with burns located
on the face would have altered facial expressions in relation
with pain.
Finally, behavioural pain scales were validated in delirious ICU patients in only two studies. A research team
from France validated the use of the BPS-NI in 30 medical or surgical ICU patients with 84% being positive for
delirium (Chanques et al., 2009) as per the Confusion Assessment Method (CAM)-ICU (Ely et al., 2001). Patients were
assessed for pain during a non-nociceptive procedure (i.e.,
catheter dressing change) and a nociceptive procedure (i.e.,
turning). Higher BPS-NI scores were found during turning
(median = 6) compared with rest (median = 3) and the nonnociceptive procedure (median = 3) (p < 0.001). The effect
size for responsiveness was large for the three items of the
BPS-NI with 3.64 for vocalisation, 2.82 for facial expression,
1.47 for upper limb movements and 3.46 for the total BPSNI scores. Recently, the use of the CPOT was validated in 40
delirious ICU patients (i.e., as per screening with CAM-ICU)
by a Canadian research team (Kanji et al., 2016). Similarly, higher CPOT scores during painful procedures (i.e.,
turning, endotracheal suctioning or dressing change) compared with baseline and a non-painful procedure (mean
difference = 3.13; p < 0.001, and effect size Cohen D = 2.0).
These study ndings suggest that the BPS-NI and the CPOT
are valid tools for the assessment of pain in ICU patients with
6
delirium; however, further testing by other research teams
is required to support such conclusions.
Assessment tools can only be shown to be valid for a specic purpose, in a determined group of respondents and in a
given context (Streiner et al., 2014). As specied in the recommendation related to BPS and CPOT in the PAD guidelines
(Barr et al., 2013), their use should be considered with caution in brain-injured ICU patients. Indeed, recent evidence
has shown that ICU patients with a brain injury affecting
their LOC appear to have different behavioural reactions to
pain, such as the absence of grimace and muscle rigidity in
most of them. Therefore, existing behavioural pain scales
may not be applicable to those patients and further adaptation of these scales may be necessary. Insufcient evidence
is available in burn patients (Wibbenmeyer et al., 2011).
However, we may anticipate that burns on the face and limbs
may affect facial expressions and limb movements which
would necessitate adaptation of existing pain scales. The
BPS-NI and CPOT appear to be valid for use in ICU patients
with delirium but this has to be replicated by other research
teams to support external validity. Yet no evidence on the
validity of the use of behavioural pain scales in ICU patients
with cognitive decit is available and research is denitely
needed.
C. Glinas
support tools on the evaluation of pain were provided to
ICU nurses, physicians and residents; pocket cards were
distributed to nurses, and posters were placed in every
patients room. After patients were assessed for pain with
the NRS or the BPS by ICU nurses, physicians were notied of a pain event (NRS > 3 or BPS > 5) or an agitation
event (RASS > 2) and could intervene accordingly. Decreases
in mechanical ventilation duration and nosocomial infection
rate were demonstrated in the intervention group (p < 0.05)
but no differences in ICU length of stay and mortality
were found. Another research team from Australia implemented the BPS along with RASS in a general ICU (Williams
et al., 2008) using a pre/post-test study design. Education on the tool use was provided to all staff. Outcomes
were documented in 369 and 400 mechanically ventilated
patients before and after the tool implementation, respectively. The proportion of ICU patients who received sedatives
with or without analgesics was greater after tool implementation (88%) than before (57%) (p < 0.001). No difference
in duration of mechanical ventilation was found between
the two groups (Williams et al., 2008). In a pre/post
prospective study from a German research team (Radtke
et al., 2012), the NRS and BPS were also implemented
along with a sedation (RASS: Sessler et al., 2002) and
delirium (Delirium Detection Score: Otter et al., 2005)
scales in three ICUs. A total of 619 ICU patients were
included i.e., 241 in the pre-training period, 228 in the
post-training period and 150 in the follow-up period. This
latter period representing the extended training (with three
consecutive educational sessions, and an ICU support team
available during the implementation phase) was compared
with standard training (one educational session of 45-minute
duration) in the post-training period and was found to
lead to more signicant changes in ICU practices (i.e.,
more frequent documentations of pain assessments) and
to their sustainability at 1-year follow-up (p < 0.01). Tool
implementation had no impact on mechanical ventilation
duration and ICU length of stay. Pain monitoring was associated with a decrease in mortality (OR = 0.35 with 95% CI:
0.140.86).
More recently, in a quality improvement project led by
Chanques team, systematic pain assessments with NRS or
BPS were completed by ICU nurses during the rst turning of
the day (De Jong et al., 2013), and appropriate pain management interventions were provided in collaboration with
physicians. Similar educational strategies (i.e., training in
small group sessions, posters) from the rst study (Chanques
et al., 2006) were used, and the clinical information system
software was updated. A total of 630 care procedures were
analysed in 193 ICU patients i.e., 53 at baseline (n = 184 procedures), 90 during implementation (n = 299 procedures) and
50 post-implementation (n = 149 procedures). The incidence
of severe pain as dened by NRS > 6 or BPS > 5 decreased
signicantly from 16% at baseline to 6% during the implementation phase, and 2% post-implementation (p < 0.05).
Incidence of at least one severe adverse event (i.e., cardiac
arrest, arrhythmias, tachycardia, bradycardia, hypertension, hypotension, desaturation, bradypnoea or ventilator
distress) also signicantly decreased from 37% at baseline to
17% during implementation, and 21% post-implementation
(p < 0.05). Patients who had severe pain were more likely to
experience a severe adverse event (OR = 2.74 (1.54; 4.89),
7
before and 32 (82%) patients after tool implementation had
recollection of their ICU stay and completed the patient
satisfaction survey. Patients reported decreased retrospective pain ratings (8.5 pre versus 7.2 post, p = 0.04) and
were satised with pain control before and after the pain
tool implementation. Fifty-three surveys (89% of all distributed) and 32 (50%) were completed by ICU nurses pre
and post-implementation of NVPS, respectively. Most nurses
(78%) ranked the tool as easy to use. Implementation of
the tool increased nurses condence in assessing pain
in nonverbal, sedated patients (57% pre versus 81% postimplementation, p = 0.02). However, no differences were
found in nurses condence in managing patients pain
before and after the tool implementation. The main barriers
described by nurses included the physicians pain management practices, personal beliefs and attitudes towards
pain, and characteristics that limit the patients ability to
self-report.
Although these study results are promising, further
research is clearly needed to evaluate the uptake of an
ICU pain management initiative by the inter-professional
team, and to measure its impact on sustainability of practice
changes and patients outcomes. Indeed, earlier studies primarily focused on the effects of clinicians training on the
use of pain assessment tools. Whether this really translates
into the day-to-day use of such tools by the ICU interprofessional team, changes in clinical practices that are
sustained over time, improved inter-professional collaboration and better patient outcomes needs to be investigated
more closely. In addition, very little is known about the
impact of such initiatives on the patients experience of pain
in the ICU and many initiatives were led by nursing teams
only (Glinas et al., 2011a; Rose et al., 2013; TopolovecVranic et al., 2010). Involving the ICU inter-professional
team in the implementation process is necessary to ensure
their collaboration and support in the pain management
process. Indeed, inter-professional collaboration is a key
component in health care delivery and can lead to better
patient outcomes (Rose, 2011). Finally, pain and sedation
assessments should be performed concomitantly as it has
been found to guide clinicians in their decision making process and to lead to better use of analgesic and sedative
agents (Chanques et al., 2006).
8
et al., 2014b; Young et al., 2006) or to remain stable during
painful ones (Glinas et al., 2011b; Sifeet et al., 2007). In
other studies, respiratory rate (RR) (Chanques et al., 2009;
Kapoustina et al., 2014) and end-tidal CO2 were found to
increase during a painful procedure (Arbour and Glinas,
2010; Glinas and Arbour, 2009), while SpO2 (oxygen saturation) was found to decrease (Boitor et al., 2015; Glinas
and Johnston, 2007). Except for associations found between
vital signs (i.e., HR, RR and SpO2 ) and the self-report of
pain in cardiac surgery ICU patients (Arbour and Glinas,
2010) and critically ill TBI patients (Arbour et al., 2014b);
vital signs failed to be related to the patients self-report of
pain (Arbour and Glinas, 2010; Boitor et al., 2015; Chen and
Chen, 2015; Glinas and Arbour, 2009; Glinas and Johnston,
2007; Kapoustina et al., 2014). Such ndings are not surprising as many other sources of distress besides pain can make
them uctuate (Herr et al., 2011).
However, as described in a wide Canadian survey, most
ICU nurses (n = 733/796, 92%) consider vital signs moderately
to extremely important for the assessment of pain (Rose
et al., 2012). Nurses need to be more aware of the evidence
showing the lack of validity related to the use of vital signs
in the ICU pain assessment process. Indeed, the recommendation in both ASPMN (Herr et al., 2011) and SCCM (Barr
et al., 2013) calls for caution with their use, and that they
should only be used as cues for further assessment of pain
with appropriate validated tools i.e., self-report measures
or behavioural pain scales.
C. Glinas
index can only be utilised in sedated patients and it would
not be applicable to patients who are awake, conscious and
unable to self-report.
Regarding pupillary reexes, pupil size signicantly
increased by 16% during a noxious procedure (i.e., endotracheal suctioning or repositioning) and returned to baseline
ve minutes after the procedure (p < 0.001) in 48 sedated
and mechanically ventilated cardiac surgery ICU patients (Li
et al., 2009). Interestingly, in a sample of 100 postoperative patients who awoke from general anaesthesia (Aissou
et al., 2012), a high positive correlation of 0.88 (p < 0.001)
was found between pain scores (5-item verbal rating scale
or VRS) and pupil dilatation reex (PDR). In patients (n = 39)
who reported a VRS > 1, PDR before and after morphine titration was 35% and 12% respectively (p < 0.001). Moreover, the
PDR threshold value of 23% was associated with a sensitivity of 91% and a specicity of 94% (Aissou et al., 2012). In a
recent study by Lukaszewicz et al. (2015), a percentage of
pupil size variation >19% was found to predict the presence
of pain by a BPS score >3 with a sensitivity of 100% and a
specicity of 77% before surgical dressing changes in 37 ICU
patients with cellulitis. Similar ndings were obtained in a
previous study by Paulus et al. (2014) in which a threshold
value of PDR >5% during a 20 mA tetanic stimulation could
predict with an AUC of 0.78 or 78% (95%CI: 0.610.91) insufcient analgesia (dened by an increase 1 point score on
the BPS) before endotracheal suctioning in 34 sedated ICU
patients. Overall, these results suggest that pupillometry
may potentially guide clinicians to adjust analgesia before
nociceptive procedures in critically ill patients.
Conclusion
Despite major discoveries in relation to pain assessment in
the critically ill adult in the last three decades, pain remains
a problem. Pain practice guidelines exist (Barr et al.,
2013; Herr et al., 2011), and their implementation into ICU
practice is urgently needed. Inter-professional ICU teams
must adjust their pain management protocols to available
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