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Intensive & Critical Care Nursing 68 (2022) 103118

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Intensive & Critical Care Nursing

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Research Article

Evaluation of pain severity in critically ill patients on mechanical ventilation

https://doi.org/10.1016/j.iccn.2021.103118 0964-3397/� 2021 Elsevier Ltd. All rights reserved.

⇑ Corresponding author at: Department of Nursing, Faculty of Health Sciences Kyorin University, 6-20-2 Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan.

E-mail address: [email protected] (Y. Ito).

Yumi Ito a,⇑, Koji Teruya b, Emiko Nakajima a

aDepartment of Nursing, Faculty of Health Sciences, Kyorin University, Tokyo, Japan bDepartment of Public Health, Faculty of Health Sciences, Kyorin University, Tokyo, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Received 22 August 2020 Revised 8 June 2021 Accepted 23 June 2021

Keywords: Pain assessment Critically ill Mechanical ventilation Intensive Care

Objectives: To elucidate how patients’ illness severity, respiratory status, or haemodynamics are associ- ated with the pain score of critically ill patients. Methods: This was an observational study of patients on mechanical ventilation after surgeries. At rest and on turning, patient pain was evaluated using the Behavioural Pain Scale (BPS) and the Critical- Care Pain Observation Tool (CPOT). Related factors were collected from medical records and analysed. Findings: Multiple logistic regression analysis was performed using data on 127 scenarios. An increase of >2 in BPS score on turning was affected by the Acute Physiology and Chronic Health Evaluation (APACHE) II score (odds ratio [OR] = 0.864), systolic blood pressure at rest (OR = 1.032), BPS at rest (OR = 0.638), heart rate difference (OR = 1.124), and tidal volume difference (OR = 0.548). An increase of >2 in CPOT on turning score was associated with the APACHE II score (OR = 0.894), Sequential Organ Failure Assessment score (OR = 1.248), systolic blood pressure at rest (OR = 1.025), heart rate difference (OR = 1.096), and tidal volume difference (OR = 0.578). Conclusion: The Behavioural Pain Scale and the Critical-Care Pain Observation Tools were associated with illness severity and haemodynamics. A reduction in tidal volume may be useful in assessing pain.

� 2021 Elsevier Ltd. All rights reserved.

Implications for clinical practice

� Elevated systolic blood pressure, increased heart rate, and illness severity were clearly associated with increased Behavioural Pain Scale or Critical-Care Pain Observation Tool scores. When assessing pain using the Behavioural Pain Scale, attention should be paid to haemodynamics and illness severity.

� The reduction in tidal volume might be used as an indicator to evaluate the patient’s pain over time in clinical nursing practice. � When assessing pain in critically ill patients using the Behavioural Pain Scale, it may be useful to add tidal volume reduction to the assessment items.

Introduction

The Behavioural Pain Scale (BPS) (Payen et al., 2001) and the Critical-Care Pain Observation Tool (CPOT) (Gélinas et al., 2006) are recommended alternative measures for pain assessment in those patients who are unable to self-report their pain (Devlin

,

et al., 2018) (Table 1 and Table 2). Nociceptive pain is the most common type of pain experienced by critically ill patients (Yvonne and Burns, 2014), and is affected by the patient’s clinical condition, tracheal intubation or treatment such as analgesia. We have reported that BPS score is significantly associated with illness severity and ventilation (Ito et al., 2017). However, to the best of our knowledge, no study has examined the relationship between CPOT and the patient’s condition.

In Japan, the clinical practice guidelines for the management of pain, agitation, and delirium in adult patients in the intensive care

Table 1 Behavioral pain scale (BPS).

Item Description Score

Facial expression Relaxed 1 Partially tightened (e.g., brow lowering)

2

Fully tightened (e.g., eyelid closing) 3 Grimacing 4

Upper limb movements No movement 1 Partially bent 2 Fully bent with finger flexion 3 Permanently retracted 4

Compliance with mechanical ventilation

Tolerating movement 1 Coughing but tolerating ventilation for most of the time

2

Fighting ventilator 3 Unable to control ventilation 4

Table 2 Critical-Care Pain Observation Tool (CPOT).

Indicator Score

Facial expression Relaxed, neutral 0 Tense 1 Grimacing 2

Body movements Absence of movements or normal position

0

Protection 1 Restlessness 2

Compliance with ventilator (mechanically ventilated patients)

Tolerating ventilator or movement

0

Coughing but tolerating 1 Fighting ventilator 2

or Vocalization (nonventilated patients) Talking in normal tone

or no sound 0

Sighing, moaning 1 Crying out, sobbing 2

Muscle tension (Evaluation by passive flexion and extension of upper limbs when patient is at rest or evaluation when patient is being turned)

Relaxed 0 Tense, rigid 1 Very tense or rigid 2

Y. Ito, K. Teruya and E. Nakajima Intensive & Critical Care Nursing 68 (2022) 103118

unit (PAD Guidelines, 2013) were adopted in 2014, and since then, the management of pain and sedation in critically ill patients has changed significantly (Barr et al., 2013).

The latest guidelines also recommend administration of light sedation and analgesia as a first-line approach (Devlin et al., 2018). As Rijkenberg et al. (2017) discuss that ‘such light sedation management needs to be taken into account when developing pain behavioral assessment tools’, analgosedation (analgesia-first seda- tion) may change the patient’s expression of pain. To the best of our knowledge, no study has examined whether BPS and CPOT are associated with physical response in critically ill patients, even under light sedation control.

In this study, we aimed to investigate the association between BPS or CPOT scores in critically ill patients and respiratory status haemodynamics and sedation scores, or illness severity indicators such as the Acute Physiology and Chronic Health Evaluation (APACHE II) or Sequential Organ Failure Assessment (SOFA) scores.

Methods

Study design and participants

This was a retrospective observational study. We used quantita- tive data for factors affecting pain assessment scores in critically ill patients on mechanical ventilation for analysis. The survey was conducted between March 2017 and September 2018 using data

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from intensive care unit (ICU) patients who were admitted in hos- pitals affiliated with medical universities in Japan.

The subjects were patients aged 20 years or older who received mechanical ventilation after surgery. Patients with cranial nerve diseases were excluded as they are prone to developing limb paral- ysis and are thought to exhibit different pain behaviour changes (Payen et al., 2001). We terminated the observation when mechan- ical ventilation was discontinued and the tracheal tube was removed, or when oral and written communication was possible.

Ethical approval

This study was approved by the Kyorin University School of Medicine Clinical Epidemiology Review Board (approval number: 374). Only patients who provided informed consent participated in this study. If the patient was on a ventilator and was unable to communicate, consent was obtained from the family or close relatives. Written consent was obtained from all patients or their family members. Only anonymised data were analysed.

Data collection

We evaluated pain at rest and on turning using the BPS and CPOT pain scales. Pain evaluation was conducted by a research observer who had completed a course at an external medical insti- tution. The Japanese version of the BPS, translated by the Japanese Society of Respiratory Care Medicine in 2007, and the Japanese ver- sion of the CPOT (CPOT-J), verified in 2016, were used (Yamada and Ikematsu, 2016). We defined ‘at rest’ as 30 minutes rest without any treatment. This duration is necessary for the reduction of stress hormones, which are increased by activity (Chanques et al., 2006; Arbour and Gélinas, 2010). Moreover, the evaluation of pain scales was performed at the time of arterial blood sampling, which was performed as a daily nursing procedure. In this study, we set turning as a ‘painful’ situation for critically ill patients, as it is considered a painful nursing care activity in the development of CPOT (Gélinas et al., 2006). Turning was defined as a change from a supine position to 30� or 45� semi-lateral position, which was performed by two nurses according to facility procedures. Pain scale scores were evaluated at the time the patient exhibited the most painful reactions on turning as described in ‘Pain assessment and pharmacological management’ (Pasero and McCaffery, 2011).

We also collected data from the patients’ medical records to determine basic attributes such as sex, underlying disease, and sur- gical procedures, as well as two scores for illness severity: APACHE II, and SOFA scores. In addition, data on sedation level (Richmond Agitation-Sedation Scale [RASS]), ventilator settings, patient infor- mation from ventilation monitors (ventilation volume, airway pressure, and respiratory rate), arterial blood gas analysis results (pH, PaO2, PaCO2, HCO3

�, SaO2), haemodynamics (blood pressure and heart rate), and the type and dosage of analgesics and seda- tives used were collected at the time of pain scale evaluations.

Statistical analysis

The difference between patients’ BPS scores ‘at rest’ and ‘on turning’ was set as the BPS difference, and the difference between patients’ CPOT score ‘at rest’ and ‘on turning’ was set as the CPOT difference. Multiple logistic regression analysis was used to inves- tigate the association between patient data and these differences. The mean BPS difference was 1.77 ± 2.036, whereas the mean CPOT difference was 1.98 ± 2.131. Accordingly, the dependent variables were set to indicate ‘increased pain’ when the BPS difference or CPOT difference had values greater than 2.0. Independent variables included sex, APACHE II score, SOFA score, RASS score, tidal vol- ume, PaCO2, HCO3

�, systolic blood pressure, and heart rate. Along

Table 4 Subject attributes (n = 127).

Variables at rest on turning Median (IQRa) Median (IQRa)

RASS (score points) �1 (3) �1 (2) Tidal volume (ml/kg) 7.39 (2.31) 6.99 (2.74) Respiratory rate (breaths/min) 16 (5) 20 (6) Systolic blood pressure (mmHg) 116.0 (31) 122 (29) Heart rate (beats/min) 77.0 (17) 80 (19) SOFA score (points) 9 (5) pH 7.45 (0.056) PaCO2 (torr) 39.5 (7.0) HCO3

� (mmol) 26.7 (6.9) PaO2/FIO2 ratio 248.5 (121.2)

a IQR: interquartile range

Y. Ito, K. Teruya and E. Nakajima Intensive & Critical Care Nursing 68 (2022) 103118

with these variables, in which differences were observed between ‘at rest’ and ‘on turning’ conditions, the respective differences in the following were also set as independent variables: RASS score, systolic blood pressure, heart rate, and tidal volume. Most of the turning was performed from the supine position to the semi- lateral position, but a small number of turns from the semi- lateral position to the supine position were also performed, so this was added as a factor in the analysis as ‘differences in turning pro- cedures’. The backward stepwise method based on the likelihood ratio test was used for the selection of variables. The goodness- of-fit for the models was determined using the Hosmer–Lemeshow test. In addition, we conducted a discriminant analysis to verify the estimated model. The significance level was set at 5%, and statisti- cal analysis was performed using SPSS Statistics 25. R Commander was used to check the multicollinearity of the variables of multiple logistic regression analysis (Kanda, 2013).

Findings

Participants’ attributes

There were 40 patients who met the criteria for screening for inclusion during the study period. We excluded four patients who had postoperative disturbance of consciousness (which was one of the exclusion criteria), and two patients whose consent could not be obtained owing to sudden hospital transfer. A total of 34 patients consented to participate in the study.

The attributes of the included patients are shown in Table 3, using the number of patients, median, and interquartile range (IQR). All study participants underwent tracheal intubation, and during the survey, ventilator settings included synchronised inter- mittent mandatory ventilation in only three cases, and the remain- der included either assist-control biphasic positive airway pressure or continuous positive airway pressure. There were 127 scenarios for which pain assessment could be performed in pairs of ‘at rest’ and ‘on turning’ conditions. The participants’ attributes are listed in Table 4.

BPS and CPOT scores

The mean BPS scores were 3.82 ‘at rest’ and 5.59 ‘on turning’. The mean CPOT scores were 1.17 ‘at rest’ and 3.18 ‘on turning’. The results of the Wilcoxon signed-rank test showed significant elevations in both BPS and CPOT scores (p = 0.000 for both BPS and CPOT) ‘on turning’ compared with those ‘at rest’. Of the 127 pairs of ‘at rest’ and ‘on turning’ situations, the BPS score difference was more than 2 in 57 pairs, whereas the CPOT score difference was more than 2 in 65 pairs.

Table 3 Subject characteristics (n = 34).

Variables n

Sex Male/Female 20/14 Clinical diagnosis Ischemic heart disease 9

Valvular heart disease 11 Aortic disease 8 digestive diseases 5 others 1

Variables Median (IQRa) Age (years) 74 (13.75) Duration of mechanical ventilation (days) 7 (12) APACHE II score (points) 24.5 (8.5)

a IQR: interquartile range

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Analysis of factors affecting BPS difference and CPOT difference at rest and on turning

The variables selected after analysis as factors affecting BPS dif- ference between ‘at rest’ and ‘on turning’ situations were APACHE II score (odds ratio [OR] = 0.864), systolic blood pressure ‘at rest’ (OR = 1.032), BPS score at rest (OR = 0.638), heart rate difference (OR = 1.124), and tidal volume difference (OR = 0.548). The Hosmer-Lemeshow test result was p = 0.543 (Table 5). The vari- ables selected as factors affecting CPOT difference were APACHE II score (OR = 0.894), systolic blood pressure ‘at rest’ (OR = 1.025), heart rate difference (OR = 1.096), tidal volume differ- ence (OR = 0.578), and SOFA score (OR = 1.248). The CPOT scores ‘at rest’ were not assessed. The Hosmer–Lemeshow test result was p = 0.588 (Table 6). Regarding the multicollinearity in the results of multiple logistic regression analysis, we confirmed that the Vari- ance Inflation Factor of all variables was less than 2.0.

In addition, we performed a discriminant analysis to examine the factors related to tidal volume reduction. The independent variables included sex, age, difference in situation, APACHE II score, SOFA score, RASS score, tidal volume, PaCO2, HCO3

�, systolic blood pressure, heart rate and difference between ‘at rest’ and ‘on turn- ing’ concerning RASS score, systolic blood pressure, heart rate, and tidal volume. Only tidal volume ‘at rest’ and systolic blood pressure ‘at rest’ were selected as significant attributes (discrimi- nant score = 0.643 � tidal volume ‘at rest’ + 0.023 � systolic blood pressure ‘at rest’ �7.555, Wilks’ Lambda = 0.847, p = 0.000).

Discussion

In this study, we examined the relationship between pain scale scores and illness severity, respiratory and circulatory status, and sedation in critically ill patients on mechanical ventilation. One researcher evaluated BPS and CPOT scores; however, the data used in the analysis were collected frommedical records after pain eval- uation was performed, and since the study observer was blinded when assessing BPS and CPOT, it can be assumed that no bias was introduced during pain evaluation.

APACHE II score, systolic blood pressure at rest, heart rate dif- ference, and tidal volume difference were selected as factors affect- ing BPS and CPOT differences. Regarding BPS and CPOT differences, the pain was seen to increase with elevation of systolic blood pres- sure ‘at rest’ or elevation of heart rate difference, whereas the pain was seen to decrease with an increase in APACHE II score or tidal volume. Moreover, SOFA score was associated with CPOT differ- ence only; CPOT difference increased with an increase in SOFA score.

Regarding vital signs, previous studies have not indicated any significant associations between BPS and CPOT scores and vital signs (Aïssaoui et al., 2005; Faritous et al., 2016; Boitor et al.,

Table 5 Factors affecting BPS of the difference between rest and turning (n = 127).

Factor b OR (95%CI) P-value

Differences in turning procedures �0.100 0.905 (0.440 — 1.862) 0.786 BPS at rest �0.449 0.638 (0.422 — 0.966) 0.034 APACHE II score �0.146 0.864 (0.794 — 0.941) 0.001 Systolic blood pressure at rest(mmHg) 0.031 1.032 (1.008 — 1.055) 0.007 PaCO2 (torr) �0.090 0.914 (0.828 — 1.010) 0.076 Heart rate difference (bpm) 0.118 1.126 (1.024 — 1.237) 0.014 Tidal volume difference (ml/kg) �0.602 0.548 (0.403 — 0.744) 0.000

Hosmer & Lemeshow test v2 = 6.973 P = 0.548. b: beta coefficient. CI: confidence interval OR: odds ratio. Dependent variable is set to indicate ‘‘increased pain” when the BPS difference > 2.

Table 6 Factors affecting CPOT of the difference between rest and turning (n = 127).

Factor b OR (95%CI) P-value

Differences in turning procedures �0.060 0.942 (0.480 — 1.848) 0.862 CPOT at rest �0.238 0.788 (0.574 — 1.082) 0.141 APACHE II score �0.112 0.894 (0.825 — 0.970) 0.007 SOFA score 0.221 1.248 (1.063 — 1.463) 0.007 RASS at rest 0.300 1.350 (0.992 — 1.836) 0.056 Systolic blood pressure at rest (mmHg) 0.024 1.025 (1.004 — 1.046) 0.021 Tidal volume at rest (ml/kg) �0.313 0.731 (0.533 — 1.003) 0.052 Heart rate difference (bpm) 0.092 1.096 (1.006 — 1.195) 0.036 Tidal volume difference (ml/kg) �0.548 0.578 (0.423 — 0.789) 0.001

Hosmer & Lemeshow test v2 = 0.528 P = 0.588. b: beta coefficient. CI: confidence interval OR: odds ratio. Dependent variable is set to indicate ‘‘increased pain” when the CPOT difference > 2.

Y. Ito, K. Teruya and E. Nakajima Intensive & Critical Care Nursing 68 (2022) 103118

2016). Patient turning, which was used as a ‘painful’ procedure in this study, is known to be the most painful procedure for critically ill patients (Puntillo et al., 2014). Conversely, critically ill patients are prone to developing haemodynamic instability, and patient turning might trigger a drop in blood pressure and development of arrhythmias (Brindle et al., 2013).

In this study, we used multiple logistic regression analysis that considered haemodynamically related factors, such as patient severity and RASS score, which allowed us to clarify the relation- ship among pain, systolic blood pressure, and heart rate. Further- more, the difference in pain rating scale scores between resting and turning was associated with resting blood pressure. This sug- gests that haemodynamics may be related to BPS and CPOT differ- ences, especially in critically ill patients who are not in circulatory failure and have a stable blood pressure.

Regarding the relationship between illness severity and pain scores, CPOT difference increased as the SOFA score increased, but BPS and CPOT differences tended to decrease as the APACHE II score increased. In this study, the SOFA score was calculated daily and used in the analysis, while the APACHE II score was the only value obtained within 24 hours of ICU admission and was used continuously throughout the analysis. Therefore, the APACHE II score did not reflect the effect of daily changes, and the two mea- sures of illness severity showed contradictory results. Most com- monly, pain experienced by critically ill patients is likely to be nociceptive and reflects an inflammatory response. Although it is possible that the pain response in critically ill patients could be modified by deep sedation, sedation was mild in this study, with a median RASS of �1. It was thought that there was a relationship between increased illness severity due to an inflammatory response and a greater pain response.

The fact that the SOFA score only demonstrated an association with the CPOT score may be attributed to the sensitivity and speci- ficity of the BPS and CPOT scores. The BPS has been reported to have higher specificity than the CPOT (BPS, 91.7%; CPOT, 70.8%),

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whereas the CPOT has higher sensitivity than the BPS (BPS, 62.7%; CPOT, 76.5%) (Severgnini et al., 2016). In the present study, we observed significant pain in many situations using the CPOT score (cut-off > 5), despite the inability to asses pain using the BPS score (cut-off > 2). This finding supports the results of the study by Severgnini et al. who concluded that the CPOT reflects the severity given by both APACHE II and SOFA scores, which is the basis of the higher sensitivity of the scale in observing changes in medical conditions. Moreover, most of our participants had undergone cardiovascular surgery, and although their biological response to surgical invasion was stable, they exhibited fluctua- tions in circulatory dynamics. Accordingly, the SOFA score reflected the circulatory score, revealing the effect of the administration of catecholamines, which likely affected the increase in the CPOT difference.

With regard to pain and ventilation volume, awake adults gen- erally exhibit an increase in respiratory rate and tidal volume due to pain (Duranti et al., 1991), and in postoperative patients, espe- cially those who undergo thoracoabdominal surgery, rapid–shal- low breathing reduces tidal volume (Ford et al., 1983; Nishino et al., 1988). Although postoperative dysfunction of the diaphragm and atelectasis are probable factors, analgesics have been reported to improve ventilation to some extent (Wahba et al., 1975). The present findings showed that when the tidal volume increases on turning, the BPS and CPOT differences indicate a trend of reduction in pain. In other words, pain is felt when the tidal volume decreases, verifying the association between pain and tidal vol- ume. In patients on mechanical ventilation, dorsal diaphragm movement decreases, and ventilation volume decreases in the supine position (Burioka, 1998), whereas turning to lateral posi- tioning is known to improve dorsal ventilation and correct the ventilation-perfusion mismatch.

In critically ill patients, turning is usually performed once every 2–3 hours (Stiller, 2000). In cases of severe lung injury, turning may reduce the ventilation-perfusion ratio. However, the patients

Y. Ito, K. Teruya and E. Nakajima Intensive & Critical Care Nursing 68 (2022) 103118

in this study had a mean hypoxemia PF ratio (PaO2/FiO2) of 263.33 torr, which meant that the degree of lung injury was mild, according to the criteria for Acute Respiratory Distress Syndrome (Force et al., 2012). Therefore, tidal volume was not directly affected by turning. Turning is one of the procedures that causes the strongest from of pain in critically ill patients (Brindle et al., 2013). In our study, the BPS and CPOT scores were elevated because of turning, indicating accompanying pain. Although turn- ing normally improves ventilation, in this study, we considered that it induced pain and temporarily reduced the tidal volume.

The BPS and CPOT include ‘patient–ventilator asynchrony’ in the sub-items to capture reactions to pain using coughing and asynchrony with the ventilator. However, modern-day mechanical ventilators are able to synchronise to spontaneous breathing to reduce asynchrony with the patient’s breathing (Kacmarek, 2011), leading to fewer patient–ventilator asynchrony warning alarms. Moreover, ventilators have also been developed to elimi- nate asynchrony with the patient, where the synchrony between the ventilator and the patient’s spontaneous breathing is further improved using closed-loop ventilation (Schulze, 2000). Conse- quently, it has become more difficult to assess pain based on asyn- chrony. Meanwhile, coughing may arise due to factors other than pain, such as stimulation of the respiratory tract by the tracheal tube and respiratory secretions. Thus, it might be difficult to assess the presence or absence of pain by using coughing or ventilator asynchrony. Gélinas et al. also expressed a similar view on the patient–ventilator asynchrony sub-item when they developed the CPOT scale (Gélinas et al., 2014). We conducted a discriminant analysis to examine the factors associated with a decrease in tidal volume, and only resting tidal volume and resting systolic blood pressure were selected as significant attributes. This finding sug- gested that a reduction in tidal volume was directly associated with pain, independent of respiratory status or sedation level.

In this study, reduced tidal volume was found to be associated with the pain scale adjusted for other factors, so it might be an index for assessing pain related to respiration, even when asyn- chrony with the respirator is not recognised during the evaluation of BPS or CPOT.

Limitations

The present study has some limitations. First, this study was conducted only in patients who had undergone surgery at a single university hospital over a limited/shorter period. Therefore, the generalisability of the results must be carefully assessed. Second, the study included a limited number of patients. Despite this, we were able to analyse almost all patients who could have been included in the study, and we believe that there is no significant selection bias. In addition, based on previous research, only turning was analysed as a painful situation, so verification in other situa- tions could not be performed.

Nevertheless, we are not aware of any other studies that have examined the relationship between pain measures such as BPS and CPOT and the pathophysiology of patients, and therefore, the implications of this observational study may be crucial.

Conclusion

We have shown that BPS score and CPOT score are significantly associated with changes in haemodynamics and illness severity, which have not been elucidated in previous studies.

In addition, a decrease in tidal volume was shown to be associ- ated with increased BPS or CPOT scores.

5

Since changes in tidal volume can be observed over time, add- ing changes in tidal volume to BPS and CPOT as an evaluation item might be useful for more appropriate pain evaluation.

Ethical approval

This study was approved by the Kyorin University School of Medicine Clinical Epidemiology Review Board (approval number 374). Only patients with informed consent participated in the study. If the patient was on a ventilator and was unable to commu- nicate, consent was obtained from family or close relatives. We analyzed only anonymized data.

Acknowledgements

We would like to express our sincere gratitude to all participants who willingly cooperated in the study and provided valuable infor- mation. We would also like to thank the nurses in ICU, and the staff of the departments of anaesthesiology, cardiovascular surgery, and gastroenterological surgery. These professionals showed utmost consideration in conducting this study.

Role of the funding source

The authors had no sources of funding to declare.

Conflict of interest

We declare no competing interests.

Contributors

YI was involved in the research design, data analysis, interpre- tation of results, and data management, and contributed to author- ing the final report. EN was involved in the research design, interpretation of results, and authoring of the final report. KT was involved in the data analysis and interpretation of results. All of the authors approved the final version of the manuscript.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.iccn.2021.103118.

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