Abstract
Objectives
Children hospitalized in a pediatric intensive care unit (PICU) are frequently exposed to distressing and painful medical procedures and interventions. There is a lack of clinical scales to measure procedural pain-related distress in ventilated children. The Behavioral Pain Scale (BPS) was initially developed to detect procedural pain in critically ill adults. This study aims to assess the BPS’s discriminant properties for measuring procedural pain-related distress in ventilated pediatric patients incorporating two instruments validated for pediatric patients.
Methods
This prospective exploratory study was performed with ventilated children admitted to the interdisciplinary 14-bed PICU of the University Children’s Hospital, University Medical Center Hamburg-Eppendorf, Germany. The nurse in charge and an independent observer simultaneously assessed the patients using German versions of the BPS, the COMFORT-B scale (CBS), and the modified Face, Legs, Activity, Cry, Consolability (mFLACC) scale immediately before and during endotracheal suctioning.
Results
We analyzed 170 parallel assessments in n=34 ventilated children. Patients were (mean ± SD) 9.5 ± 4.8 years old. Internal consistency for the BPS was excellent (α=0.93). We found a high rater agreement for all clinical scales (BPS: k=0.73, CBS: k=0.80, mFLACC: k=0.71). Strong correlations were identified between BPS and CBS (r=0.89) and BPS and mFLACC (r=0.79). The BPS cutoff values showed likewise excellent results (area under the curve CBS >16: 0.97; mFLACC >2: 0.91).
Conclusions
In our population of ventilated children, the BPS was well suited to detect procedural pain-related distress compared with two validated pain scales. Further extensive validation studies should follow to support our findings.
Introduction
International guidelines for children’s intensive care treatment recommend adequate analgesia and sedation [1], [2], [3], [4], [5]. Considering that mechanically ventilated children in pediatric intensive care units (PICUs) undergo more than twice as many distressing and painful procedures (e.g., suctioning, vascular cannula placement, lumbar puncture, and blood sampling) as non-ventilated patients, this is particularly relevant [6, 7]. Acute procedural pain may have immediate effects on the current medical condition of the patient, including hemodynamic stability, intracranial pressure, and metabolism. Pain-related experiences also correlate with the development of chronic pain syndromes, posttraumatic stress disorder, and low health-related quality of life [8]. Therefore, avoiding unnecessary painful procedures and providing adequate pharmacological and non-pharmacological measures for necessary painful procedures should always constitute health care professionals’ primary objective. Ideally, predicting the response to painful stimuli should be possible, e.g., by objective pain and sedation monitoring to titrate analgesic and sedative therapy accordingly before the noxious intervention as needed [9, 10]. Pending extensive evaluation of these predictive methods, it is essential to assess current procedural pain-related distress adequately by clinical scales that have shown to produce valid scores to provide adequate analgesia then.
Self-report is considered an ideal source for the assessment of pain intensity [11]. However, in most cases, self-reporting is not possible in endotracheally intubated and ventilated children. In this respect, clinical pain scales provide an objective method of pain assessment. A recent systematic review found 65 pain scales developed for pediatric patients; however, only 28 were considered suitable based on the availability of construct validity, internal consistency, and interrater reliability [12]. Despite this large number of scales, pain scores of only six scales, including the COMFORT-scale [13] and the Face, Legs, Activity, Cry and Consolability (FLACC) scale [14], have been validated in ventilated term infants, toddlers, and children [15]. Here, these scales were evaluated in the context of acute, postoperative pain. Many international guidelines recommend the COMFORT scale, the COMFORT- B Scale (CBS), or the FLACC scale for preverbal infants and children in the PICU unable to self-report [1, 3], [4], [5]. Both scales produced valid scores when assessing acute and postoperative pain in critically ill children [15]. Today, the (modified) FLACC and the CBS are the most commonly used scales in PICUs [18]. The FLACC scale [14] represents the most commonly used behavioral observational scale for pain in pediatric patients in general [16]. It was initially developed for the detection of postoperative pain. Recently, good reliability and sensitivity for detecting procedural pain were shown in pediatric patients undergoing painful interventions in the emergency department [17]. Since the rating of the item “cry” is a challenge in intubated patients [18], the item was changed to “cry (ventilated children)” in the modified FLACC (mFLACC) [19]. The COMFORT scale was initially developed to assess distress in pediatric intensive care patients 0–18 years of age [13]. Because of the physiological measures’ poor reliability and validity [20], a modified version of the COMFORT scale is now available, including only the behavioral measures, referred to as the CBS [21]. Subsequent studies also showed that the CBS provided valid pain scores compared to the Visual Analog Scale, the Numerical Rating Scale [22, 23], or the FLACC scale [24, 25] in postoperative patients. Nevertheless, none of the above scales’ pain scores have been validated to assess procedural pain or distress in critically ill infants and children on mechanical ventilation. However, their use for this purpose is widespread in daily clinical practice [26].
Outside the context of the PICU, two pain scales have been specifically developed to assess acute and procedural pain in infants and children: The Modified Behavioral Pain Scale (MBPS) [27], an adaptation of the Children’s Hospital of Eastern Ontario Pain Scale [28], and the EVENDOL scale [29]. However, the MBPS was developed to assess pain during immunization of infants, and the EVENDOL was developed for acute and procedural pain of infants and children in the emergency department. None of these scales were evaluated in ventilated pediatric patients.
Observational studies indicate that, contrary to current recommendations, pediatric patients unable to self-report may not always receive regular pain assessment [30, 31]. Reasons for this might include lack of satisfaction with the previous scales [31], for example, because they are considered too complex for routine use [32], [33], [34]. If the time required for the use of clinical pain scales and documentation of results is high, the likelihood of adoption and regular use is low [35]. Subsequently, inadequate pain assessment in children may result in underestimation and under-treatment of pain [36].
The Behavioral Pain Scale (BPS) was developed in 2001 by Payen et al. as an easy-to-use pain assessment scale to explicitly detect procedural pain in sedated, mechanically ventilated adults [37]. The BPS proved excellent validity and reliability for detecting procedural pain in several studies in adult patients on mechanical ventilation [38], [39], [40]. International guidelines recommend the BPS for monitoring pain in adult intensive care patients who cannot self-report [8]. The scale has only been used in two studies to assess pain in pediatric patients [31, 41]. Nevertheless, these studies do not provide enough evidence to confirm the validity of the scores to measure pain and pain-related distress in children. However, the BPS is already being used in children [30].
Pain is defined as both a sensory and emotional experience [42]. The response to a noxious stimulus, assessed with clinical observational scales, thus includes both pain intensity and behavioral distress [43]. Distress can be summarized as all negative experiences associated with pain, anxiety, and fear [13, 44]. Some studies suggest that available scales may have difficulty distinguishing pain-related behaviors from other distress-related behaviors [45, 46]. The distinction between pain vs. distress is not a clear-cut matter, and there are good reasons not to disentangle these often-coexisting concepts entirely [44]. Similarly, common pain scales are assumed to be most likely a measure of pain-related distress, a composite of pain and non-pain factors, rather than a measure exclusively of pain [47].
The aim of the present study was to evaluate the established, short, and straightforward BPS used to measure procedural pain in adult intensive care patients for the assessment of procedural pain-related distress in ventilated pediatric patients.
Methods
Patients
With the approval of the local ethics committee (approval code: PV5210; Ethics Committee of the Medical Association of Hamburg, Germany), this prospective observational study was conducted in the 14-bed PICU of the University Children’s Hospital, University Medical Center Hamburg-Eppendorf, Germany, between March 2017 and September 2018. Written informed consent was obtained from both parents of patients involved in the study. Patients were mechanically ventilated and received continuous analgesic and sedative therapy. A neuromuscular block, neuromuscular disease, or traumas to the peripheral or central nervous system were defined as exclusion criteria.
Clinical scales
The BPS consists of three behavioral items: facial expression, upper limb movement, and compliance with mechanical ventilation (Table 1). Each item is scored from 1 to 4 so that the overall BPS ranges from 3 (no pain) to 12 (maximum pain) [40]. A BPS score >5 indicates pain in adult patients [48]. The CBS assesses the behavioral characteristics of alertness, calmness/agitation, respiratory response, physical movement, muscle tone, and facial tension, with scores ranging from 1 to 5 for each item, resulting in a minimum score of 8 and a maximum score of 30. A CBS score of >16 indicates pain [21]. According to the acronym, the FLACC considers five behavioral characteristics: face, legs, activity, cry, and consolability. Each item is rated from 0 to 2. Thus, the scale ranges from 0 (no pain) to 10 (worst pain) [49]. An FLACC of >2 indicates that the patient is experiencing pain [24]. The FLACC was modified to the mFLACC by changing the criterion “crying” to “cry (ventilated children)” for the use in ventilated pediatric patients.
Behavioral pain scale.
| 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 |
We used German language versions of the BPS [50], CBS [51], and FLACC scale [52] for this study. The German versions of the scales were translated backward by the authors to ensure the equivalent description of the individual items. In the case of the mFLACC scale, we added the translations of “ventilated child” and “facial expression” to the German version of the FLACC scale accordingly (Appendix S2). Prior to the study, the nursing staff was trained in using the BPS and mFLACC scale. The CBS was already part of the local standard of care; hence its use was familiar for the PICU staff.
Study protocol
Patients received treatment according to the hospital’s standards, which included sedative and analgesic therapy according to the PICU’s standard protocol (Appendix S1). For the study purpose, we selected regular endotracheal suctioning as a noxious stimulus. Patients were assessed after a rest period without intervention or disturbance within the preceding 30 min, immediately before (t0, pre-stimulation), and during stimulation by endotracheal suctioning (t1, stimulation). Depending on the length of stay in the PICU, multiple endotracheal suctioning events were evaluated. Endotracheal suctioning was performed using a closed system according to local treatment standards.
The nurse in charge and an independent observer (MM or FU; 4th-year medical students) assessed each patient using German versions of the BPS, the CBS, and the mFLACC scale. The scales were randomly applied using a randomization list before each suctioning and assessed independently by both observers, one after the other.
Statistical analysis
The BPS’s internal consistency was calculated using Cronbach’s alpha, the interrater reliability was assessed using Cohen’s weighted kappa. Finally, we determined repeated measures correlations [53] between individual scores to account for the repeated assessments in patients. The Wilcoxon signed-rank test and linear mixed-effect models (considering multiple measurements) [54] were calculated to analyze the changes in BPS scores across the different time points (t0, t1). Cutoff values discriminating between pain and no pain (based on CBS >16 or mFLACC >2) were determined by calculating receiver operating characteristic (ROC) curves. p-Values less than 0.05 were considered significant. Statistical analyses were performed using R 4.1.1 (R Core Team, Vienna, Austria) and IBM SPSS Statistics (Version 27.0. Armonk, NY, USA).
Results
Patient characteristics
This study initially included n=38 patients admitted to the PICU for various reasons (Table 2). Patients were (mean ± SD) 9.5 ± 4.8 years old, were on mechanical ventilation for 14.2 ± 15.8 days, and stayed for 19.0 ± 18.8 in the PICU. Table 2 shows detailed patient characteristics. Three patients were excluded secondarily: In two patients, no assessment was possible before extubation or transfer to another unit; we excluded the third patient because of previously unknown neuromuscular disease.
Clinical characteristics of the included patients (n=34).
| Sex | |
| Female | 16 (47.1) |
| Male | 18 (52.9) |
| Age, years | 9.5 ± 4.8 |
| Bodyweight, kg | 31.1 ± 17.0 |
| Time on mechanical ventilation, days | 14.2 ± 15.8 |
| Length of PICU stay, days | 19.0 ± 18.8 |
| Mode of mechanical ventilation | |
| SIMV | 32 (94.1) |
| BIPAP | 2 (5.9) |
| Diagnostic group | |
| Postoperative (non-cardiac) | 12 (35.3) |
| Miscellaneous (including injury) | 11 (32.3) |
| Respiratory | 6 (17.6) |
| Gastrointestinal or renal | 2 (5.9) |
| Cardiac postoperative | 1 (2.9) |
| Survival | |
| Yes | 32 (94.1) |
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BIPAP, bilevel positive airway pressure; PICU, pediatric intensive care unit; SIMV, synchronized intermittent mandatory ventilation. Continuous variables are shown as mean ± SD, and counts as n (% of all included patients).
Out of a total of 194 suctioning events, 24 events were excluded because of no or only partial assessment of scales or protocol violation (e.g., manipulation during the rest period). After exclusion, a median (interquartile range, IQR) of 2 (1–3) assessments in n=34 patients resulted in a total of 170 assessments that were included in the analysis (Figure 1). Eighty-four assessments were made pre-stimulation (t0) and 86 assessments during stimulation by endotracheal suctioning (t1). The median (IQR) scores of the respective scales assessed at t0 were BPS: 3 (3–4), CBS: 6 (6–9), and mFLACC: 0 (0–1). At t1, median scores were: BPS: 4 (3–6), CBS: 9 (6–12), and mFLACC: 1 (0–3). Before stimulation (t0), 6% of patients had a BPS >5, 3.6% had a CBS >16, and 10.7% had an mFLACC >2. At t1, 27.8% of patients had a BPS >5, 14% had a CBS >16, and 25.6% had an mFLACC >2.
Consort flow chart of included assessments.
Consistency and reliability
The internal consistency for the BPS was α=0.937. The interrater reliability of the BPS (k=0.73), the CBS (k=0.80), and the mFLACC scale (k=0.71) was high.
Correlations and discriminant validity
Strong correlations between the BPS and both the CBS (t0: r=0.72, confidence interval [CI]95%: 0.55–0.83; t1: r=0.92, CI95%: 0.87–0.96; p<0.01) and the mFLACC (t0: r=0.73, CI95%: 0.56–0.84; t1: r=0.86, CI95%: 0.74–0.91; p<0.01) were identified (Table 3). There was a significant difference between patients’ BPS scores at rest (t0) and during the intervention (t1; Wilcoxon signed-rank test, z=−5.3, p<0.01, n=84, effect size r=0.58). We also found a significant difference for the change in BPS scores between t0 and t1. We calculated linear mixed-effects models to consider the multiple measurements in individual patients with the patient ID as a random effect (Table 4).
Sensitivity and specificity
Applying the CBS pain criterion (CBS >16), a BPS cutoff score between 5 and 6 to detect pain with a sensitivity of 1 and a specificity of 0.88 was determined. Applying the mFLACC pain criterion (mFLACC >2), we calculated a BPS cutoff score between 3 and 4 to detect pain with a sensitivity of 1 and a specificity of 0.63. The ROC area under the curve (AUC) was 0.97 (CI95%: 0.94–1.0) for detecting pain by the CBS (Figure 2) and 0.91 (CI95%: 0.87–0.96) by the mFLACC scale (Figure 3).
Receiver operating characteristic curve of Behavioral Pain Scale with CBS >16 as the state variable.
Receiver operating characteristic curve of Behavioral Pain Scale with modified Face, Legs, Activity, Cry, Consolability score >2 as the state variable.
Reliability and correlations of the BPS.
| Interrater reliability | |||
|---|---|---|---|
| Clinical scale | BPS | CBS | mFLACC |
| Cohen’s weighted kappa, k | 0.73 | 0.80 | 0.71 |
| Repeated measures correlations | |||||
|---|---|---|---|---|---|
| CBSt0 | CBSt1 | mFLACCt0 | mFLACCt1 | ||
| BPSt0 | r rm (CI95%) | 0.72 (0.55–0.83) | – | 0.73 (0.56–0.84) | – |
| p-Value | <0.001 | – | <0.001 | – | |
| BPSt1 | r rm (CI95%) | – | 0.92 (0.87–0.96) | – | 0.86 (0.74–0.91) |
| p-Value | – | <0.001 | – | <0.001 | |
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BPS, Behavioral Pain Scale; CBS, COMFORT-B scale; CI95%, 95% confidence interval; mFLACC, modified Face, Legs, Activity, Cry, Consolability scale; rrm, repeated measures correlation.
Linear mixed-effects models for the change in BPS between t0 and t1.
| Predictors | Estimates | CI | p-Value |
|---|---|---|---|
| (Intercept) | 3.67 | 3.25–4.09 | <0.001 |
| t1 |
1.18 |
0.75–1.61 |
<0.001 |
| Random effects | |||
|
|
|||
| σ 2 | 2.04 | ||
| τ 00 PID | 0.62 | ||
| ICC | 0.23 | ||
| N PID | 34 | ||
| Observations | 170 | ||
| Marginal R2/Conditional R2 | 0.116/0.322 | ||
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BPS, Behavioral Pain Scale; CI, confidence interval; ICC, intraclass correlation; PID, patient ID.
Discussion
This study aimed to determine the discriminant properties of the BPS for measuring procedural pain-related distress in ventilated pediatric patients during endotracheal suction. The BPS showed excellent performance for assessing procedural pain-related distress compared with two pain scales validated for assessing acute and postoperative pain in ventilated pediatric patients, with excellent internal consistency and high interrater reliability. Furthermore, the high correlation between the BPS scores and the CBS and mFLACC scores proved good construct and concurrent validity. With high sensitivity and specificity, the BPS showed different cutoff values for the pain criterion of CBS and mFLACC. In our study, a cutoff value for the detection of pain-related distress of >5 was shown for the BPS based on the pain criterion of CBS >16. This finding corresponds to the cutoff of the BPS for unacceptable pain found in conscious sedated adult patients [48]. The BPS’s AUC for discriminating pain-related distress compared to the two other applied scales was excellent.
The BPS has only been used in two studies in children [31, 41]. The study by Akinci et al. was an efficacy study investigating remifentanil vs. fentanyl infusions for postoperative analgesia in 22 children and used the BPS to measure pain on an assumption of validity [41]. A defined BPS target score of 3 was used to titrate the analgesic therapy. The authors concluded that remifentanil infusion provides comparable analgesia to fentanyl infusion in mechanically ventilated postoperative pediatric patients. However, the study did not address the BPS’ discriminant properties, and no other pain scale was used to test for criterion validity. The study by Sulla et al. investigated the applicability of the Italian version of the BPS in n=9 mechanically ventilated infants less than one year of age by comparing the BPS with the CBS [31]. Both scales were assessed before, during, and after painful (mobilization and tracheobronchial aspiration) and non-painful interventions. In total, the study showed a good correlation between the BPS and the CBS and good discriminant properties of the BPS. The authors also applied a questionnaire for physicians and nursing staff on pain measurement in their PICU. In this survey, 60% of the respondents expressed dissatisfaction with current pain scales (mainly CBS and Numerical Rating Scale). Nevertheless, the overall perception of the BPS was positive.
In particular, for the assessment of procedural pain-related distress in the context of pediatric intensive care, a short and easy-to-record scale is needed. Thus, the advantage of the BPS is its simplicity [31, 55]. It includes only three assessment criteria compared to the six and five criteria of the CBS and mFLACC. This simplicity may improve the frequency of pain-related distress assessments in critically ill pediatric patients on mechanical ventilation. Nonetheless, sufficient observation time must be maintained even if the BPS is shorter and easier to evaluate. If the observation period is too short, there is a considerable risk of underestimating the patient’s pain [56]. However, a clinical scale that is easy to assess and interpret could improve regular assessment of pain and distress in ventilated children in the PICU [34], especially for procedural pain-related distress.
Children treated in PICUs experience a variety of distressing or painful procedures in addition to the already stressful environment [6, 7]. Assessment of pain and determining the appropriate analgesia/pain balance remains a particular challenge in ventilated children. The clinical evaluation depends on the assessor’s experience, so clinical pain scales can help to objectify the assessment. Evaluation of the psychometric properties of existing pediatric behavior-based pain scales for assessing procedural pain is the subject of ongoing research [17, 57]. These studies provide support for the use of procedural pain assessment in pediatric patients through verification of reliability and construct validity. However, there is still a lack of respective studies for the unreserved use of the corresponding scales in ventilated critically ill children.
The procedure of endotracheal suctioning is considered one of the most painful procedures in a PICU in the literature, aside from punctures and intubations [58], [59], [60], [61]. Then again, this assumption is based on scores derived from clinical pain scales. As stated in the introduction, these scales likely also measure other distress-related behaviors in addition to pain-related behaviors. A significant proportion of our group of pediatric patients also responded to endotracheal suction with pain according to the used scales. Through this observation alone, this intervention cannot be reliably characterized as explicitly painful. Although fear and anxiety are, in fact, rather unlikely under the sedative therapy in our study, indicated by the low CBS before intervention (t0), they cannot be completely ruled out as a factor in the reaction to the suction maneuvers. Likely, the distinction between pain and distress cannot be fully achieved through observable behaviors [17]. Therefore, future studies should focus on the capacity of observational scales to differentiate pain and distress in ventilated pediatric children. Distinguishing these entities could improve the therapeutic approach by adjusting care and targeting titration of either analgesic or sedative therapy, depending on whether pain or distress is the primary concern.
To this point, no instrument was developed to measure procedural-related distress in critically ill infants and children on mechanical ventilation, and the use of existing pain scales is pending validation studies. However, scales explicitly developed and validated for those patients are urgently needed. The promising results of our study bring the BPS into play as a straightforward procedural-related distress scale in ventilated pediatric patients. More extensive studies to validate the psychometric properties of the BPS in ventilated pediatric patients are needed to confirm our results.
Limitations
The sample of patients recruited was very heterogenous in terms of age, underlying disease, and medication. However, our patient selection reflects the broad spectrum of patients treated in a PICU. We performed multiple measurements in patients. These were considered in the statistical analysis using repeated measures correlations and mixed-effects models. We sought to select a challenging part of routine care with sufficient intensity to provoke patient reactions but to avoid additional discomfort in these vulnerable patients. Regardless, endotracheal suctioning in pediatric patients may not be an optimal stimulus to differentiate between pain and distress. Future studies should test construct validity by comparing painful and non-painful interventions and examining responsiveness to analgesia. These studies should also investigate the discriminatory power of the BPS to distinguish between distress and pain. Nurses ought to be interviewed about the usability of the BPS, and the time taken to assess the scales should be compared. Future studies should also validate the German-language adaptations of the BPS, CBS, and mFLACC used in clinical practice for accurate translation and cultural adaptation.
Acknowledgments
The authors would like to thank the “Hamburg macht Kinder gesund e.V.” foundation for supporting this study. We would also like to thank Dr. Benedikt Claus of the PedScience Research Institute for providing statistical consultation.
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Research funding: The study was supported by the foundation “Hamburg macht Kinder gesund e.V.”. The foundation had no role in the design and conduct of the study.
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Author contribution: Maximilian D. Mauritz and Felix Uhlenberg conceptualized and designed the study, collected data, conducted initial analyses, and reviewed and revised the article. Vito Giordano helped to merge the data and reviewed and revised the article. Larissa A. Dreier helped conceptualize and design the study, conduct statistical analyses, and review and revise the article. Dr. Deindl conceptualized and designed the study, designed the data collection instruments, coordinated and supervised data collection, and provided critical reviews of the article for important intellectual content. All authors approved the final article as submitted and agree to be accountable for all aspects of the work.
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Competing interests: Authors state no conflict of interest.
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Informed consent: Informed consent has been obtained from all parents of patients included in this study.
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Ethical approval: Research involving human subjects complied with all relevant national regulations, institutional policies and is in accordance with the tenets of the Helsinki Declaration (as amended in 2013), and has been approved by the Ethics Committee of the Medical Association of Hamburg, Germany (approval code: PV5210).
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