Abstract
Purpose
Diaphragm function is rarely studied in intensive care patients with unit-acquired weakness (ICUAW) in whom weaning from mechanical ventilation is challenging. The aim of the present study was to evaluate the diaphragm function and the outcome using a multimodal approach in ICUAW patients.
Methods
Patients were eligible if they were diagnosed for ICUAW [Medical Research Council (MRC) Score <48], mechanically ventilated for at least 48 h and were undergoing a spontaneous breathing trial. Diaphragm function was assessed using magnetic stimulation of the phrenic nerves (change in endotracheal tube pressure), maximal inspiratory pressure and ultrasonographically (thickening fraction). Diaphragmatic dysfunction was defined by a change in endotracheal tube pressure below 11 cmH2O. The endpoints were to describe the correlation between diaphragm function and ICUAW and its impact on extubation.
Results
Among 185 consecutive patients ventilated for more than 48 h, 40 (22 %) with a MRC score of 31 [20–36] were included. Diaphragm dysfunction was observed with ICUAW in 32 patients (80 %). Change in endotracheal tube pressure and MRC score were not correlated. Maximal inspiratory pressure was correlated with change in endotracheal tube pressure after magnetic stimulation of the phrenic nerves (r = 0.43; p = 0.005) and MRC score (r = 0.34; p = 0.02). Thickening fraction was less than 20 % in 70 % of the patients and was statistically correlated with change in endotracheal tube pressure (r = 0.4; p = 0.02) but not with MRC score. Half of the patients could be extubated without needing reintubation within 72 h.
Conclusion
Diaphragm dysfunction is frequent in patients with ICU-acquired weakness (80 %) but poorly correlated with the ICU-acquired weakness MRC score. Half of the patients with ICU-acquired weakness were successfully extubated. Half of the patients who failed the weaning process died during the ICU stay.
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Introduction
Intensive care unit (ICU)-acquired weakness (ICUAW) is a complication observed in critically ill patients that combines myopathy and neuropathy [1–3]. Its incidence varies but may rise up to 100 % in patients with multiorgan failure [4, 5]. It is associated with delayed weaning from mechanical ventilation (MV) [6], longer ICU stay, frailty and poor outcome [7, 8]. The diaphragm, the main inspiratory muscle, is also a victim of critical illness. However, the extent of diaphragmatic dysfunction compared to limb muscle weakness during critical illness is a matter of debate [9, 10]. Some studies have indeed reported particular diaphragm sensitivity to aggression while others have reported the opposite [11–13]. MV by itself has been proven to impair diaphragm force (a term labelled ventilator-induced diaphragmatic dysfunction) and to promote diaphragm atrophy in the critically ill [14–17] without affecting limb muscles [14, 18].
Weaning from the MV in ICUAW patients may be difficult, and studying the potential diaphragmatic dysfunction in these patients is therefore of interest. To date, two studies have explored the relationship between ICUAW and diaphragm dysfunction using a pulmonary function test at the bedside [maximal inspiratory pressure (MIP)] [19] or electromyography [20] and reported conflicting results. Using a dedicated cutting edge multimodal tool combining magnetic stimulation of the phrenic nerves, diaphragm ultrasound and pulmonary function tests to study diaphragmatic function at the bedside, we designed this study with the aim of assessing the diaphragm function in ICUAW patients undergoing a spontaneous breathing trial (SBT). We hypothesized that such dysfunction would be associated with ICUAW.
Methods
Design
The physiological prospective study, approved by the Comité de Protection des Personnes Sud-Méditerranée, Nîmes, France (2013-AA00487-38) and registered on clinical trial.gov (NCT01968889), was conducted over a 6-month period from May to November 2013 in a 16-bed medical and surgical ICU. Given that this study did not modify current diagnostic or therapeutic strategies, the need for written consent was waived according to the French Law (Law 88–1138 relative to Biomedical Research of December 20, 1988 modified on August 9, 2004).
Patients
Patients were eligible for inclusion in the study if they were diagnosed for ICUAW [defined by a Medical Research Council (MRC) Score <48] [1, 4, 21] and mechanically ventilated for at least 48 h and were undergoing a spontaneous breathing trial (SBT) as a step towards separation from the ventilator [22]. Routine MRC score evaluation by physiotherapists has been implemented in daily practice for years in our unit. Patient screening was performed jointly by the ICU physiotherapist and the main investigator (PHM) [1, 4].
Non-inclusion criteria were: contraindication to magnetic stimulation of the phrenic nerves (cardiac pacemaker or implanted defibrillator, cervical implants) [15, 16]; pre-existing neuromuscular disorders; cervical spine injury; bihemispheric or brain stem lesions; impossibility to assess muscular strength in a limb because of amputation or immobilization [1, 4].
Demographic data, severity scores, comorbidities, risk factors for ICUAW, reasons for admissions to the ICU and for initiating MV were prospectively recorded. The duration of mechanical ventilation, duration of ICU stay and ICU mortality were also collected.
Diaphragm assessment
Inspiratory muscle strength was assessed during a SBT both in T-tube and with a pressure support ventilation of 7 cmH2O and a PEEP level of 0 cmH2O in 20–30° upright position by three methods: magnetic stimulation of the phrenic nerve [12, 15, 16], maximal inspiratory pressure (MIP) [19] and ultrasonographically (diaphragm excursion and thickening fraction) (Fig. 1).
Bilateral supramaximal magnetic twitch stimulation of the phrenic nerves and its subsequent change in endotracheal tube pressure (Ptr,Stim) was used as previously described to approximate diaphragm function independently of the patients participation [12, 15, 16]. It is considered the gold standard to evaluate diaphragm function and serves as the reference method in this study. Briefly, patients were studied in a semi-recumbent position [23] and, after disconnection from the ventilator, they were allowed to exhale until the expiratory airflow reached zero. The tracheal tube was then occluded and tracheal pressure measured during the stimulation. The tracheal tube occlusion lasted approximately 5–10 s. Diaphragmatic dysfunction was defined by a Ptr,Stim <11 cmH2O [16, 19, 24].
MIP was recorded following a maximum inspiratory effort against a closed airway without using a unidirectional valve permitting exhalation [19]. Ultrasound evaluation allowed the evaluation of thickness of the diaphragm after careful observation of the end of inspiration and expiration on real-time graphs of airflow and airway pressure. Measurements were averaged over at least three respiratory cycles. Diaphragmatic thickness was assessed in the zone of apposition of the diaphragm to the rib cage between the 8th and 10th intercostal spaces using a 7.5- to 10-MHz probe [25, 26]. Briefly, thickness at end-expiration (TEE, mm) and at the end-inspiration (TEI, mm) were measured for at least three breaths to calculate the diaphragm thickening fraction as (thickness at the end-inspiration − thickness at the end-expiration)/thickness at the end-expiration) and expressed as a percentage. A thickening fraction below 20 % was considered a surrogate of diaphragmatic dysfunction [25] and 30 % was considered a surrogate to predict weaning success [27].
Weaning and postextubation care
According to existing guidelines and expert opinions, ICUAW patients were extubated by the physician on service if they succeeded the SBT [9, 22, 28]. Extubation was systematically followed by prophylactic non-invasive ventilation according to our protocol [29, 30]. Reintubation was performed in cases of respiratory, neurological or cardiovascular failure according to the guidelines [9, 28] and following local protocol [31].
Endpoints
The primary endpoint was, on the day of the SBT, to assess whether evaluated ICUAW was associated with diaphragmatic dysfunction defined by a Ptr,Stim below 11 cmH2O. Secondary endpoints were to assess whether ICUAW and diaphragmatic dysfunction were associated with extubation failure, defined as a need for reintubation within 72 h after extubation.
Statistical analysis
Statistical analysis was performed with MedCalc® software (v.11.1; Ostend, Belgium; ). The number of subjects needed was calculated to detect at least a 0.4 Spearmann correlation coefficient between MRC score and Ptr,Stim. Forty subjects were needed to test this hypothesis with a power of 0.8. Quantitative variables were expressed as mean (and standard deviation) or median (and interquartile 25–75 %) and compared using Student’s t test or the Wilcoxon test as appropriate. Categorical variables were expressed as numbers (%) and compared using the Chi-square test or the Fisher test as appropriate. A p value below 0.05 was considered significant.
Results
During the 6-month study period, 185 patients were ventilated for more than 48 h of whom 40 were consecutively enrolled in the study (Fig. 1; Table 1). Evaluation and SBT took place 9 days [6–15] after the initiation of MV and 38 patients were subsequently extubated. At the time of evaluation, MRC was 31 [20–36] (Figs. 2, 3). Two patients underwent a tracheotomy without any extubation attempt; they were categorized as weaning failure patients.
Assessment of diaphragm function in ICUAW patients
Magnetic stimulation of the phrenic nerves and its subsequent variation in tracheal pressure (Ptr,Stim) was used as the reference measure to diagnose diaphragmatic dysfunction in the study. Among the 40 patients with ICUAW included in the present study, 32 (80 %) showed signs of diaphragmatic dysfunction (Table 1; Fig. 2). There was no correlation between Ptr,Stim and MRC score (Fig. 2).
The day of the SBT, MIP was obtained for 40 patients and was equal to 18 cmH2O [13–25], significantly lower in patients with diaphragmatic dysfunction compared to patients without diaphragmatic dysfunction (Table 1) and values reported in healthy volunteers [19, 32]. MIP was correlated both with Ptr,Stim (r = 0.46; p = 0.003) and MRC score (r = 0.31; p = 0.05) (Fig. 3a).
Ultrasound evaluation of the diaphragm during SBT is summarized in Table 1. Diaphragm exploration was completed by thickening fraction, a surrogate of the work of breathing [26, 34] and a predictor of weaning success [27]. In the present study, 23 patients among 32 (70 %) with criteria of ICUAW presented a thickening fraction below 20 % and 28 (85 %) below the threshold of 30 % [27]. The thickening fraction was statistically correlated with Ptr,Stim (r = 0.47; p = 0.006) but not with MRC score (Fig. 3a, b).
Outcome
Among the 40 patients included, 20 were successfully extubated and 20 failed the weaning process (18 were extubated but needed reintubation within 72 h and 2 were tracheotomised after SBT failure) (Figs. 2, 3, 4). Among the 13 patients (33 %) who died during the ICU stay, 10 presented signs of diaphragmatic dysfunction the day of SBT. Weaning failure in patients who presented signs of ICUAW was associated with a 50 % mortality rate. Ptr,Stim was 4.3 cmH2O [3–9] the day of the SBT in patients who were ultimately reintubated and 6.8 cmH2O [4–13] (p = 0.08) in patients who were not reintubated (Table 2). MIP measurement the day of SBT was not associated with the need for subsequent reintubation and was 16 cmH2O [12–23] versus 20.5 cmH2O [14–27], p = 0.3, in patients who needed to be reintubated versus patients who were successfully extubated. Among the ultrasound criteria, thickening fraction was associated with extubation success. Thickening fraction was 12 (6–15 %) versus 20 % (13–38 %), p = 0.008 in patients who needed to be reintubated versus patients who did not (Table 2).
Discussion
This study shows for the first time an association between diaphragmatic dysfunction and ICUAW in critically ill patients during weaning. In a prospective cohort of 40 patients presenting signs of ICUAW defined by an MRC score of 48 or less, symptoms of diaphragmatic dysfunction, evaluated using phrenic nerve magnetic stimulation, ultrasound and pulmonary function tests were present in 80 % of the patients (Figs. 2, 3). Half of the patients were weaned from the ventilator without being reintubated within 72 h, while the mortality rate in those patients who failed the weaning process was 50 % (Fig. 4). This highlights the need to better identify the patients who will not be weaned in this ICUAW population.
Our study presents some limitations. First, ICUAW was diagnosed in all patients and we were therefore unable to study diaphragmatic dysfunction in patients without ICUAW. Second, weaning was studied as a secondary endpoint and the study was not powered to predict factors independently associated with weaning success. Identifying these factors in the ICUAW population is challenged by the complexity and heterogeneity of critically ill patients. This highlights the necessity to tailor our weaning strategy based on a personalized physiologic assessment level. Third, ICUAW was diagnosed using MRC score and after ruling out other causes of limb weakness than critical illness. Although MRC accuracy has been questioned [35], it is reproducible [36, 37] and routinely performed by trained physiotherapists as a screening tool in our ICU. Furthermore, electromyography is currently not recommended when clinically detected weakness can be related to no other plausible cause than critical illness [1, 3]. Fourth, during the ICU stay or upon admission, most of the patients in the present study presented an infection (Table 1), a risk factor for both ICUAW and diaphragmatic dysfunction [3, 12, 15].
We report that 32 out of 40 (80 %) experienced diaphragmatic dysfunction the day of SBT using the Ptr,Stim threshold of 11 cmH2O after magnetic stimulation of the phrenic nerves (Fig. 2). This method is currently the gold standard to evaluate strength of the diaphragm at the bedside because it does not need the patients’ participation [15, 16, 19]. We report values comparable to other studies performed in patients with duration of mechanical ventilation of more than 1 week [15, 38, 39] with no reported ICUAW [40]. Ultrasound evaluation of the diaphragm showed a similar incidence of diaphragmatic dysfunction, from 64 to 80 %, depending on its definition (Table 1; Fig. 3a, b). The intensity of ICUAW was not correlated with the degree of diaphragmatic dysfunction evaluated by magnetic stimulation or by ultrasound (Figs. 2, 3b). Despite sharing the same cellular pathways [41–43], both injury and repair of the diaphragm and limb muscles seem to be differently affected during critical illness with previous medical history, metabolic/nutritional disturbances, sepsis, shock, surgery, immobilization being the most reported factors associated with atrophy and contractility [11–13].
MIP showed a significant correlation (r = 0.31; p = 0.05) with MRC score (Fig. 3a), consistent with the findings of De Jonghe et al. [44]. MIP measurement should be interpreted not as a specific surrogate of the diaphragm but rather as a global inspiratory muscle assessment involving also the accessory muscles and the patients capacity to participate in the function test [19].
The aim of the present study was to evaluate diaphragm function in ICUAW patients and we only described succinctly the weaning outcome of these patients. Almost half of the patients included were successfully weaned from the ventilator despite showing signs of ICUAW and diaphragm dysfunction (Figs. 2, 3, 4).
In conclusion, in a prospective cohort of 40 critically ill patients with ICUAW and an MRC score below 48 the day of the spontaneous breathing trial, while 32 (80 %) also presented diaphragmatic dysfunction detected using multimodal evaluation of the diaphragm. There was no correlation between the MRC score and the degree of the diaphragmatic dysfunction evaluated by magnetic stimulation. Half of the patients were successfully weaned from the ventilator but mortality in the half that failed the weaning process was 50 %, highlighting the need for further studies aiming to predict weaning success or failure in this very high risk population.
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Boris Jung reports personal fees from Merck (Whitehouse Station, NJ, USA) and Astellas (Tokyo, Japan) without relations with the present study. Samir Jaber reports personal fees from Maquet, Draeger, Hamilton Medical, Fisher Paykel and Abbott without relations with the present study. Pierre Henri Moury, Martin Mahul, Audrey De Jong, Fabrice Gallia, Albert Prades, Pierre Albaladejo, Gerald Chanques and Nicolas Molinari have nothing to disclose related to the subject of the article.
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This study was supported by University Hospital of Montpellier.
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B. Jung and P. H. Moury contributed equally to this study.
Clinical Trials.gov Identifier: NCT01968889.
Take-home message: We report for the first time the evaluation of diaphragm function and related outcome in a prospective study performed in 40 consecutive patients with ICU-acquired weakness (MRC score < 48) among 185 consecutive patients ventilated for more than 48 h.
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Jung, B., Moury, P.H., Mahul, M. et al. Diaphragmatic dysfunction in patients with ICU-acquired weakness and its impact on extubation failure. Intensive Care Med 42, 853–861 (2016). https://doi.org/10.1007/s00134-015-4125-2
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DOI: https://doi.org/10.1007/s00134-015-4125-2