A simplified lung ultrasound approach to detect increased extravascular lung water in critically ill patients

The early evaluation of haemodynamic status and need for fluid treatment are essential in the management of patients presenting with severe cardio-pulmonary failure, both those who are spontaneously breathing and those who are mechanically ventilated [1].

Accurate assessment and monitoring of haemodynamic status often require the placement of a pulmonary artery catheter or other invasive vascular lines. Trans-pulmonary thermodilution is often used for measuring volumetric haemodynamic parameters, of which the most commonly used are the global end diastolic volume and extra vascular lung water (EVLW) [2, 3]. This procedure is based on a central venous access and femoral arterial line, without the need for pulmonary artery catheterization.

The change in EVLW is a useful parameter for monitoring the evolution of cardiogenic pulmonary oedema, acute lung injury and acute respiratory distress syndrome (ARDS). In previous studies, the EVLW index showed a statistically significant correlation with PaO₂/FiO₂ ratio in ARDS patients [4].

In recent years, ultrasonography has shown to be useful as a “new eye” to look inside the lung [5, 6]. A change in the balance between air and fluids in the lung parenchyma determines a significant and corresponding change in the acoustic patterns that can be easily detected and measured.

After studying the artefacts that the air/fluid imbalance creates, it is possible to diagnose some pulmonary conditions, ranging from lung consolidations to an increased interstitial water content [7]. The B-lines are vertical echoic comet-tail artefacts detected by lung ultrasonography, and they are typically correlated with the loss of pulmonary aeration and an increase in lung water [8].

Lichtenstein was the first who published about B-lines as a sign of interstitial lung water in 1997 [9].

In 2004, Jambrik et al. published the first paper showing the use of lung ultrasonography to assess interstitial lung water in the lung [10].

In 2005, Agricola et al. found a good correlation between the number of B-lines at lung ultrasonography and EVLW in a selected group of 20 post-operative cardiac surgery patients [11]. Their data demonstrated, for the very first time, a correlation between lung ultrasonography and invasive measurements of EVLW. However, the limitation of their study was that the data were obtained from only a specific subgroup of post-surgical patients that represents a minority of the population usually submitted to invasive haemodynamic monitoring in the intensive care unit (ICU). Moreover, the ultrasound technique proposed in their study is quite time consuming, which has also been suggested by recent evidence-based recommendations [7].

In the years following these studies, more studies have showed the ability of lung ultrasonography to reliably assess lung water or, in general, the aeration of the lungs [12, 13].

In 2015, Zhao et al. showed a very good correlation between lung ultrasound score (LUS) and EVLW, as measured using trans-pulmonary thermodilution, in a population of 21 ARDS patients [14].

The aim of our study is to evaluate the correlation between B-lines and EVLW in a general population of mechanically ventilated ICU patients. Moreover, a further aim is to assess the possibility of using a very simplified ultrasound approach based on a technique that is easily reproducible at the bedside.

Nineteen consecutive adult patients requiring mechanical ventilation and haemodynamic monitoring with trans-pulmonary thermodilution were enrolled in the study.

In all patients, lung ultrasound examination was feasible. The median number of chest quadrants positive for B-lines was 4 (range 0–8). The median EVLW index was 10 ml/kg actual body weight (ABW) (range 4–20) and 11 ml/kg PBW (range 6–22). A significant correlation was found between the number of positive quadrants at lung ultrasound examination and EVLW index (rho = 0.612 and p = 0.0053 for ABW; rho = 0.493 and p = 0.032 for PBW) (Figs. 1, 2).

The detection of more than 3 positive chest quadrants upon lung ultrasound examination showed the best specificity (70%) and sensitivity (100%) for predicting an EVLW index >10 ml/kg ABW (area under ROC curve: 0.894; 95% CI 0.668–0.987, p < 0.0001, see Fig. 3).

Detection of more than 4 positive chest quadrants at lung ultrasound examination showed the best specificity (100%) and sensitivity (50%) for predicting an EVLW index >10 ml/kg PBW (area under ROC curve: 0.8; 95% CI 0.556–0.945, p = 0.0048, see Fig. 4).

Our study confirms the correlation between B-lines and EVLW in critically ill patients with various haemodynamic conditions and diseases. Moreover, we found that the presence of more than 3 B-line positive chest quadrants correlates well with EVLW superior to the threshold of normality when EVLW is indexed for the actual body weight. When using the predicted body weight, as is what is reported in some papers in the literature, the number of B-line positive quadrants that best predicts EVLW >10 ml/kg was 4.

In recent years, ultrasonography has been increasingly used in daily practices in the ICU and has showed its usefulness in monitoring the pulmonary aeration and haemodynamic condition of critically ill patients [14, 15]. Haemodynamic evaluation using a bedside ultrasound offers a large number of advantages to invasive monitoring, including the absence of risks, not needing costly disposable devices, and rapid and easy repeatable assessments.

Some studies demonstrated the reliability of ultrasound evaluation in detecting lung oedema.

A seminal study by Agricola et al. showed a good correlation between lung ultrasound B-lines and EVLW measured by trans-pulmonary thermodilution. This method is widely used in haemodynamic monitoring and is minimally invasive in comparison to pulmonary artery catheterization because of its capability to measure not only “pressures” but also “volumes.” Extravascular lung water is one of the many important parameters that become available when this technique is applied at the bedside, and it is universally considered as one of the most important parameters to predict the real haemodynamic status and response to treatment of the critically ill. The potential of lung ultrasound examination to predict EVLW allows for the hypothesis that it can be used as an alternative to invasive procedures when the PiCCO methodology is not yet available at the bedside, as it usually occurs in the emergency setting before admission to the ICU. The study of Agricola et al. already demonstrated the correlation between the invasive EVLW and B-lines, but it evaluated only a selected population of post-operative cardiac surgery patients and excluded patients with lung diseases. In our opinion, this selection prevents the generalization of the results of the study to other patient populations. In a similar study, our group assessed the correlation between a positive lung ultrasound examination for B-lines and high EVLW or wedge pressure in a wide and multifaceted population of critically ill patients using a multi-centre enrolment scheme [16]. While Agricola et al. used a time consuming chest count of B-lines to find the linear correlation with EVLW, Volpicelli et al. applied only a dichotomous evaluation based on the positivity of lung ultrasound evaluation for B-lines, without investigating a numeric correlation between the artefacts and EVLW values.

Our study was designed to evaluate a general ICU population requiring mechanical ventilation and haemodynamic monitoring, without exclusion criteria. For this specific reason, but compatible with our sample size, our results may be better generalized to the real practice of a polyvalent ICU and in general to emergency and critical care medicine. Moreover, the ultrasound technique that we applied in our study, the simple counting of positive chest quadrants, is less labourious than Agricola’s technique but still allows for the analysis of a linear numeric correlation between the artefacts and EVLW values.

We chose 10 ml/kg as a cut-off value for an elevated EVLW index, which is in agreement with previous literature [17]. Only one of our patients with an EVLW index >10 ml/kg showed a PaO₂/FiO₂ >200. This observation is a further demonstration that EVLW has a very close association with clinically relevant gas exchange impairment.

One practical application of our limited fast lung ultrasound examination at the bedside may be in the extreme emergency setting, when the critically ill patients are still in the very early initial phase of diagnostic evaluation. In this situation, lung ultrasound examination may be very helpful in confidently ruling out the condition of elevated EVLW, possibly allowing the treating physician to be more confident in applying an intensive fluid treatment, when indicated, and in monitoring the effect on pulmonary function [18]. The new appearance of B-lines during this early phase may be considered a sign of rapidly increasing EVLW, which is a condition that demands for a stop in fluid administration [19]. On the other hand, a positive lung ultrasound examination with more than 3 or 4 positive quadrants at the very early stage should lead to a more careful consideration of the haemodynamic state before any definitive conclusion is made on the fluid treatment.

A great limitation of our study is the relatively low number of patients enrolled. The significance of our results should be read under this limited perspective. However, while we cannot exclude that increasing the number of enrolled patients may have a significant influence on the best numeric correlation between the lung ultrasound cut-off and elevated EVLW, our data represent a further confirmation of the tight relationship that exists between B-lines and EVLW detected by the PiCCO technique.

In conclusion, we showed a correlation between the number of lung quadrants positive for the presence of B-lines at lung ultrasound examination and extravascular lung water. We also showed that the detection of more than 3 B-line positive chest quadrants, when using ABW for indexing EVLW, or more than 4 B-line positive chest quadrants, when using PBW, allows for the prediction of abnormal EVLW value, with strong sensitivity and specificity. Results from our study support the use of lung ultrasonography as a screening tool in the emergency and critical care settings with an acceptable performance at the bedside in identifying patients without a significant condition of increased EVLW, with encouraging rapidity and reliability.