Can diaphragmatic ultrasonography performed during the T-tube trial predict weaning failure? The role of diaphragmatic rapid shallow breathing index

This study provides evidence that the substitution of VT with DD in the calculation of RSBI could represent an important alternate to conventional weaning predictors in a mixed population of ICU patients. Weaning indices are relevant from a clinical perspective. Indeed, patients should be extubated as soon as they are able to sustain the load of breathing to avoid ventilator-associated diaphragmatic dysfunction, infections, and increased length of ICU and hospital stay [38, 39]; on the other hand, re-intubation leads to a worse patient outcome, though the link between failing an extubation and poor hospital outcomes is associative in nature and not known to be causal [3]. Interestingly, patients failing the weaning attempt exhibited higher length of ICU and hospital stay and mortality (Table 2). An ideal predictive index should reflect all pathophysiological pathways that may lead to weaning failure, including excessive mechanical workload imposed on the respiratory muscles, impaired diaphragmatic function, weaning-induced cardiac failure, and a reduced ability to keep the airways opened and to clear secretions. Most of these pathways lead to rapid shallow breathing, which explains the rationale of taking into account the ratio between RR and VT in the study by Yang and Tobin [24]. Rather surprisingly, in our patients who failed the weaning attempt, the RSBI was much lower (63 (range, 37–90) breaths/min/L) than the threshold value of 105 to predict weaning failure described in the original paper by Yang and Tobin [24]. However, several other studies have reported a wide range of predictive values for RSBI, which may reflect differences in methodology, classification of outcomes, and patient populations [22, 40]. The relationship between inspiratory muscle fatigue and RSBI has been previously questioned. Tobin et al. [23] showed that patients develop rapid and shallow breathing almost immediately with the beginning of weaning, well before muscular fatigue could develop. Hence, they speculated that the RSBI reflects more the instauration of a compensatory mechanism to avoid respiratory muscle fatigue then fatigue itself. Thus, it is likely the rapid shallow breathing expresses the balance between mechanical load posed on the inspiratory muscles and the inspiratory muscles ability to face it. By substituting VT with DD in the calculation of RSBI we proposed a new index (the D-RSBI) that was independently associated with weaning failure and whose diagnostic accuracy was superior to the one of RSBI and other weaning predictors (DD and MIP). We speculate that the D-RSBI was more accurate because DD reflects more closely the diaphragmatic function as compared to VT. In fact, in the presence of diaphragm dysfunction, the diaphragm movement is depressed and the accessory muscles assume a greater role in generating VT [29, 30]. In these circumstances, the VT is less linked to diaphragm function than DD, which reflects the ability of the diaphragm to generate inspiratory volume and, hence, the true diaphragmatic contribution to VT [41].

Many experts consider the rationale for predicting weaning outcome very modest compared to clinical judgment, based on careful inspection [20–22]. Indeed, most weaning predictors have not withstood the test of time and the debate on the usefulness of weaning predictors is a classical topic in intensive care, since the seminal editorial by Milic-Emili [42]. However, while careful clinical observation remains the most important step in the decision to extubate, integrating it with the result of a relatively easy to obtain index like the D-RSBI (also considering the increasing use of ultrasonography at the bedside in critically ill patients) could at least support the clinician in their decision.

Diaphragmatic ultrasonography is a painless, easy to perform, non-invasive, and bedside tool [15, 43, 44] not requiring patient collaboration. The examination requires standard ultrasonography equipment, largely available in most ICUs. Diaphragmatic M-mode ultrasonography has recently been applied in healthy individuals [16, 45] and in patients undergoing a SBT [19] to measure DD, i.e., the amount of diaphragm excursion during spontaneous or assisted breathing (Fig. 2). In our patients, DD was significantly higher in the successfully than in the unsuccessfully weaned patients (Table 2). However, when we compared the diagnostic accuracy of DD compared to other weaning predictors, including D-RSBI, RSBI, and MIP, we found that the D-RSBI was superior to DD. This confirms the usefulness of D-RSBI as an index that reflects not only the diaphragm function but also the presence of rapid swallow breathing, a sign of overall imbalance between respiratory load and the ability to face it during the SBT. Kim and coworkers [19] compared the accuracy of DD versus RSBI to predict weaning failure and found that they were similar, though the AUROC was relatively narrow for both indices (AUROC ranging from 0.61 to 0.68 for DD; AUROC?=?0.58 for RSBI). This seems to confirm that the accuracy of DD is greatly enhanced when it is combined with RR in the D-RSBI. However, it is difficult to compare our results with those of Kim et al., since in the study by Kim et al. [19] the weaning failure rate was very high (above 66 %) compared to our findings; we speculate that this was due to the fact that that Kim and coworkers studied a population of patients already classified as “difficult to wean” whereas our patients were at the first weaning attempt.

Diaphragmatic dysfunction has been previously associated with muscle atrophy, cardiac failure, depletion of energetic substrates, and septic shock [46–49]. Sepsis has been reported to be associated with diaphragm dysfunction related both to myopathy and neuropathy and damages are both functional (specific force generation) and morphological (atrophy). In our study, DD was lower in patients with sepsis compared to those with other pathologies. These results are in keeping with those of Jung et al. [48] and Demoule et al. [45] who demonstrated that in septic patients there is a preferential loss of diaphragm muscle volume compared to psoas.

Our study has some limitations. First, one may argue that ultrasonography is an operator-dependent technique. However, we assessed the intra-observer and inter-observer reproducibility of DD measurements and found that ICC for both these parameters was well above 0.75, a threshold indicating a very good performance. This further confirms the results of previous studies showing good agreement of intra-observer and inter-observer reproducibility for diaphragmatic ultrasonography [16, 34, 50]. Second, our DD measurement was performed on the right hemidiaphragm. We chose, on the basis of other reports [49, 50], not to measure the left hemidiaphragm displacement because the spleen offers a small acoustic window and because gastric or colic meteorism often impairs diaphragmatic imaging on the left side. Third, DD was not re-evaluated in the weaning failure group. Such information could be helpful in determining whether weaning failure has its roots in diaphragmatic dysfunction or has a cardiac or a respiratory origin. Further studies are needed to evaluate this relevant aspect in patients failing a weaning attempt. Fourth, we failed to assess the cause of weaning failure in our patients. As an example, it is conceivable that some of our patients with pre-existing cardiac dysfunction could have failed weaning trial for “cardiac” reasons [51–53], whereas chronic obstructive pulmonary disease (COPD) patients could have failed for “respiratory” reasons. However, we believe that the D-RSBI index is likely to explore the balance between the mechanical load posed on the diaphragm and its ability to face it, and thus it can be applied whatever the physiopathological mechanism is that disrupts this balance. Fifth, since our patients were awake, we cannot exclude that they over-breath during the sonographic examination, providing falsely greater DD values. However, measurements were performed in patients with a Richmond Agitation and Sedation Scale (RASS) score ranging between –1 and +1. Furthermore, deep, superficial, or irregular breaths were excluded from the measurements and, to reduce the measurement errors, every recording was performed three times and averaged. Finally, we did not include acutely brain-injured patients as these patients usually fail due to airway compromise rather than respiratory mechanics [54]. D-RSBI may not be generalizable to this patient population.