Pain is a frequent event in intensive care unit (ICU) patients, with an incidence of moderate to severe pain during the ICU stay of up to 50% in medical as well as surgical patients 123. Pain is associated with acute stress response including changes in heart rate, blood pressure, respiratory rate, neuro-endocrine secretion and psychological distress, such as agitation 45. It has recently been reported that improved pain management was associated with improved patient outcome in the ICU 1678. However, pain remains currently under-evaluated and under-treated 39101112. Therefore, pain management is highly challenging in the ICU setting.

One of the most common painful procedures in ICU patients is moving and turning for nursing care procedures (bathing, massage of back and pressure points, sheets change, repositioning) 313. Pain during the first turning of the day is especially challenging to manage in our ICU. Indeed, this is often the longest turning time and includes the highest number of mobilizations and nursing care procedures. Moreover, the early morning nurses often have to manage ICU patients in collaboration with a reduced medical night-shift staffing, leading to necessarily greater nurse autonomy 14. For instance, it has been reported for the past decade that between 50% of patients in the USA 9 and 80% in Europe 315 received no extra medication even though pain intensity increased during that procedure. More recently, a study assessing 330 turnings in 96 medical-surgical patients reported that the pain score significantly increased between rest and turning, while a bolus of analgesic was used in less than 15% of the turnings 16. Moreover, serious adverse events (SAE) related to moving complex ICU patients are poorly documented. These SAE could be determined by the mobilization itself and/or the stress response associated with pain.

The present study was conducted to test the hypothesis that the implementation of a quality improvement process for pain management while moving ICU patients would be associated with a decreased incidence of both severe pain and SAE, and that those SAE would often be associated with pain events.

The main findings of this quality improvement project are that moving an ICU patient for nursing care procedures is associated with severe adverse events (SAE) in one out of three procedures. The incidence of at least one SAE (cardiac arrest, arrhythmias, tachycardia, bradycardia, hypertension, hypotension, desaturation, bradypnea or ventilatory distress) is strongly associated with severe pain in multivariate analysis. A healthcare quality improvement project of pain management, while moving ICU patients, is associated with a decrease in both severe pain and SAE.

Being moved for nursing care procedures is one of the most painful procedures experienced by the patient during the ICU stay, whatever the type of admission (medical, surgical or trauma) 3131633. Nevertheless, except for trauma and surgical patients, moving is currently not considered a painful procedure by ICU healthcare workers and physicians 34. Similarly, to our knowledge, no study has reported yet whether pain might be a barrier for active mobilization in ICU patients and if a specific analgesia given to decrease pain while moving ICU patients would be associated with a greater chance to achieve rehabilitation objectives in the ICU setting 3536.

One of the reasons not to treat pain is that ICU physicians may be uncomfortable ordering analgesic drugs 37 because of frequent organ dysfunction, altered pharmacokinetics and pharmacodynamics, and impaired mental status in critically ill patients 38. Indeed, adverse events have been reported in critically ill patients even with non-opioid WHO's step-1 analgesics, such as acetaminophen 39 and nefopam 40. In the present study, analgesics were administered upon nurse discretion but were chosen among eligible analgesics ordered by physicians according to the context and for each patient. Decreased incidence of severe pain and increased rate of analgesic administration observed during adjusted and consolidated steps of the quality project suggests that collaboration between nurses and physicians, which was the aim of educational intervention at the adjusted step, improved regarding appreciation of patients' pain and analgesics needs. A multidisciplinary discussion involving nurses and physicians/pharmacists is recommended regarding the complex management of pain in ICU patients 41. To better define a rational plan for a given patient, it is important for physicians to assess nursing issues as it should be important for nurses to understand the benefit and risks associated with every analgesic ordered by physicians.

Tramadol was the only drug that's use significantly increased through the study. Except in the case of severe renal impairment, tramadol is an opioid associated with a minimal risk of ventilatory depression 42. This could explain the preference of the team regarding its use in ICU patients who are at high risk of ventilatory depression. Similarly, tramadol use significantly increased in a previous quality improvement project aimed at reducing pain at rest in ICU patients 1. In that study, incidence of pain significantly decreased through the quality improvement project as well as the duration of mechanical ventilation 1. Similarly, in the present study, incidence of severe pain decreased as analgesic drug use increased without any increase of SAE. That could be attributed to an accurate evaluation of the benefit:risk ratio associated with analgesic ordering. Also, the incidence of moderate pain did not significantly decrease throughout the study. Actually, complete suppression of pain could be difficult or impossible in ICU patients considering the pain syndromes (surgery, trauma, acute pancreatitis) or contraindication of analgesic drugs in critical-illness (acetaminophen and liver dysfunction, anti-inflammatory drugs and renal dysfunction). In this way, American guidelines recommended defining an acceptable threshold of pain according to the context for each patient 43.

In order to reduce the risk of such drug adverse events, non-pharmacological therapies were developed throughout the study. Despite the implementation of music therapy as a new technology available for every patient and despite specific educational interventions, there was an increased use of non-pharmacological therapy but this increase was not sustained during the third phase of the study. Music therapy was poorly implemented throughout the project. Some nurses reported that the time which was required for a music therapy session (40 minutes) did not allow for easily preventing or treating procedural pain contrary to analgesic drugs. Also, nurses should have been more comfortable with analgesic drug use as the quality-improvement project was developed and might have discarded non-pharmacological therapies at the same time for different reasons including trust in their efficacy, timing and so on. If positive effects of music therapy and standard music listening have been shown in small-sized physiological studies in critically ill patients 4445, the feasibility and impact of larger routine implementation has yet to be evaluated. Moreover, obstacles to widespread use of non-pharmacological therapy rather than analgesic drugs need to be explored because the rationale for development of non-pharmacological therapy in critical care is strong.

Decreased pain-associated stress response could partly explain the decrease of SAE observed during the last two studied phases (adjusted intervention and consolidation P-D-C-A-steps). Pain induces reflex responses that may alter respiratory mechanics and increase cardiac demand via tachycardia and increased myocardial oxygen consumption, leading to desaturation and blood pressure changes. Stress response may also induce hypercoagulability, immunosuppression and persistent catabolism 45. In the present study, multivariate analysis adjusted to cofactors, such as severity of illness showed that severe pain events were an independent risk factor of SAE. This was confirmed by the sensitivity analysis, removing the most common pain-related adverse events (tachycardia and hypertension). Use of analgesics may decrease stress response in critically ill patients 4647. In our study, the main SAE observed were oxygen desaturation and ventilator distress (Table 4). The rate of these SAE decreased throughout the study, although ventilator management or oxygenation practices were not changed, contrary to pain management practices.

This study constitutes an improvement in quality and safety in healthcare. Such processes are fundamental to improving our healthcare, by changing our systems, avoiding overuse of ineffective care and underuse of effective care 48. Quality improvement methods, such as the Plan-Do-Check-Adjust cycle, seek to apply proven treatments and recommended strategies to "real world" patients, allowing the integration of "best evidence" and "clinical evidence" 2022. To our knowledge, there are no published data regarding the feasibility of a quality improvement process for moving ICU patients. Changing practices is challenging in an ICU setting, with necessary education of a large team 4950. Moreover, a multidisciplinary approach is essential, placing responsibility with the team rather than with individuals. Differences in pain appreciation among physicians, nurses and assistant nurses are well known in the ICU setting 34 and were found again in our questionnaire. It has been previously reported that ICU physicians under-evaluated patients' pain compared to nurses 51, and that ICU nurses under-evaluated patients' pain compared to assistant nurses 52.

Our study has several limitations. First, there were less missing data in the third phase (adjusted intervention P-D-C-A phase) than in the two first phases. This could be explained by a high workload during February and September 2010, much higher than in April 2011. Indeed, one-third of the unit had to be closed unexpectedly in April after Phase 3 had begun. To deal with missing data and to avoid a possible bias due to more frequently evaluating patients in pain in the two first phases, patients were randomly enrolled in Phase 4. This phase (consolidation of P-D-C-A-steps) was aimed to reinforce the results observed in the previous phase 2123. Second, pain was evaluated by the bedside RN (BPS) or by the patient with the help of the bedside RN (NRS), and not by an independent investigator. However, this design is appropriate in a quality improvement process of routine care because self-evaluation of the caregiver is part of the improvement process 2253. Moreover, even if it was not possible to have an independent investigator at the bedside for all 16 patients during the turning every morning, the presence of an observer could have introduced another bias leading to more accurate care 32. In this way, the study sheets were de-identified regarding the RN to allow for more independent evaluation of care. Also, the study design requires including all consecutive turnings within one month to deal with a possible punctual Hawthorne effect and to transform it in an acquired routine process 32. The findings of this quality study can be supported by the incidence of SAE, which were objectively evaluated and also decreased along with the incidence of severe pain through the study. Third, if the global impact of educational interventions was supported by a decreased incidence of pain and SAE along with an increased rate of analgesic administration, no qualitative method was performed to better assess the impact of each aspect of educational interventions on health caregivers' skill regarding pain management as well as nurse-physician interaction and nurse autonomy 1454. Finally, pain management during other nursing and medical procedures (tracheal suctioning, central intravenous line placement...) was not evaluated. This should be a further step in our quality improvement project.

A focused quality improvement project on pain management in the ICU was associated with improved pain management during patient turning for nursing procedures as determined by 1) a decreased incidence of severe pain; 2) an increased use of analgesic drugs; 3) a decreased incidence of serious adverse events. Careful documentation of pain management while moving ICU-patients for nursing procedures could be implemented as a health quality indicator in the ICU-setting.

• Moving an ICU patient for nursing care procedures is associated with serious adverse events in one out of three procedures.

• Serious adverse events are strongly associated with severe pain during these procedures.

• Health quality improvement of pain management is associated with a decrease of both severe pain and serious adverse events.

• Careful documentation of pain management while moving ICU patients could be implemented as a health quality indicator in the ICU setting.

BPS: Behavioral pain scale; BPS-NI: non-intubated BPS; COGAR: Comité d'Organisation et de Gestion de l'Anesthésie Réanimation du Centre Hospitalier Universitaire de Montpellier; ICU: Intensive care unit; NRS: Numeric rating scale; RASS: Richmond Agitation Sedation Scale; RN: Registered nurse; SAE: Serious adverse event; SAPS: Simplified Acute Physiological Score; WHO: World Health Organization

The authors declare that they have no competing interests.

GC, SJ, SDL, CG and MPS conceived the study and participated in its design and coordination. ADJ and NM performed the statistical analysis. ADJ, GC and SJ drafted the manuscript. MC and BJ helped to correct the manuscript. JC was in charge of English editing. All authors read and approved the final manuscript.