Feasibility of basic transesophageal echocardiography in hemorrhagic shock: potential applications during resuscitative endovascular balloon occlusion of the aorta (REBOA)

The porcine model is commonly used in cardiovascular research related to experimental models of hemorrhagic shock [1, 2]. Swine are mammalian vertebrates with a cardiovascular system that is very similar to humans, and for this reason, have served as the dominant animal model for previous study designs published in the literature [3, 4]. For instance, with regard to vascular size, an 80–100 kg swine has an aortic diameter of 1.6–1.8 cm versus an aortic diameter of 1.6–2.4 cm in a similarly-sized human [1, 5]. However, several potentially significant differences exist. For example, porcine hearts are shaped more like a “valentine,” have different orientations for insertion of the superior and inferior vena cava, and have dissimilar atrial components [5]. Table 1 summarizes some anatomical differences between swine and humans.

Transesophageal echocardiography (TEE) is an invasive diagnostic modality that carries minimal risk but requires extensive knowledge about anatomy, physiology, and physics for appropriate application [6]. There are numerous studies in the cardiovascular literature that have employed TEE in swine models, but nearly all of these studies have dealt with cardiovascular physiology related to cardiac surgery [7], valvular abnormalities [8], myocardial infarction [9, 10], or cardiopulmonary resuscitation [11]. Data regarding the use of TEE in swine models is limited; one of the few papers describing the technique was published over 20 years ago [2], and baseline anatomical and hemodynamic parameters for TEE use in swine models have only recently been defined [1]. Both three-dimensional [8] and transthoracic ultrasound [12] in swine models have been described, but use of basic TEE in a swine model of hemorrhagic shock has not. Herein, we describe our experience using basic multiplane TEE to characterize hemodynamic changes in a large closed chest experimental swine model of non-compressible hemorrhage using resuscitative endovascular occlusion of the aorta (REBOA). The primary aim of this study is to describe an echocardiographic method that can be used with relative ease to qualitatively assess cardiovascular function in a porcine hemorrhagic shock model.

Basic TEE exams were performed in all 15 swine. The mean animal weight was 79.6 ± 5.5 kg. Heart rate significantly increased after REBOA inflation (76.8 [S.D. 21.3] vs. 151 [S.D. 47.1]; p < 0.001) with a corresponding significant increase in shock index, but mean arterial blood pressure did not change significantly. Qualitative basic TEE findings are summarized in Table 2.

With the exception of mean pulmonary artery systolic pressure in the 2-h experimental groups, no significant changes were observed in pulmonary artery pressures despite echocardiographic findings indicating hypovolemic shock. Similarly, there were no statistically significant differences in mean arterial blood pressure in any of the three study arms prior to and after REBOA inflation, despite experimental blood loss of 40%. In all animals, basic TEE qualitatively revealed increased LV function and hypovolemia as evidenced hyperdynamic physiology.

In a convenience sample (two animals from each group), advanced functional cardiovascular measurements were obtained before and after REBOA inflation for comparison with qualitative assessments. Mean ejection fraction (EF) decreased from 64% (S.D. 9.6) to 62.1 (S.D. 16.8) after hemorrhage and REBOA inflation (p = 0.76); fractional area of change (FAC) decreased from 49.8 (S.D. 9.0) to 48.5 (S.D. 13.6) after hemorrhage and REBOA inflation (p = 0.82). VTI and LVOT measurements were obtained in animals; mean cardiac output was 3.7 L/min prior to hemorrhage and REBOA inflation, and 7.6 L/min thereafter.

Midesophageal aortic long and short axis views were obtained to confirm correct REBOA catheter position (Figs. 2, 3, and 4). Catheter position was verified in all animals with basic TEE and confirmed with the use of fluoroscopy.

In a porcine closed chest experimental swine model of non-compressible hemorrhage using REBOA, use of basic multiplane TEE detected hemodynamic changes that could not be verified with the use of mean arterial pressure and pulmonary artery catheter data. With the increasing use of REBOA in both experimental settings and clinical settings, methods to rapidly and accurately assess hemodynamics are required. The use of basic TEE is of interest to laboratory investigators and clinicians for several reasons. First, the goal of basic TEE is intraoperative monitoring; while TEE is invasive, at the basic level, TEE can be used by a wide variety of scientists and clinicians to observe hemodynamic changes associated with aortic occlusion and hemorrhage. Second, basic TEE may reveal earlier evidence of hypovolemia despite relatively normal vital signs. Third, basic TEE may be helpful for localizing and confirming REBOA position. The primary goal of the basic TEE exam is intraoperative monitoring. The exam is not designed for practitioners to use the full diagnostic potential of TEE; hence, training requirements are considerably less than required for the advanced TEE exam [6]. Performance of basic TEE may be feasible in a wide variety of settings, including the laboratory, intensive care unit, and austere medical environments. Currently, “certification” is only available for licensed physicians who have passed an exam and demonstrated supervised performance of exams, but such requirements do not preclude performance of basic TEE exams in the laboratory by properly supervised investigators.

Limited application of TEE is potentially useful in both experimental and clinical settings where REBOA is employed for hemorrhage control because cardiac dysfunction is common in critical illness, but the effects on porcine and human hearts during REBOA are uncertain [20]. Basic TEE was feasible for all animals in our study. Clear evidence of hypovolemia was observed in all animals despite normal systemic and pulmonary blood pressure measurements. In animals with prolonged balloon inflation, evidence of early diastolic dysfunction was also observed, although in the subset of animals where EF and FAC were measured, no statistically significant differences were observed. These findings indicated a hyperdynamic cardiovascular state consistent with compensated shock. Such findings would be of great importance for both laboratory investigators and clinicians because further decreases in heart function would likely signify the upper limit of REBOA insertion before instituting definitive blood component resuscitation and surgical correction of hemorrhage.

An additional advantage of using basic TEE is for confirmation of proper REBOA location when fluoroscopic methods are not available. In previous studies, the subxiphoid view from a Focused Abdominal Sonogram for Trauma (FAST) was shown to reliably identify a central aortic guidewire, but in situations where the abdomen or chest is opened, such an exam may not be practicable [21]. In austere or limited resource settings when REBOA may be required as a temporizing measure for severe hemorrhage, fluoroscopy will likely be unavailable whereas a modern, compact TEE machine might be. In our study, a portable ultrasound machine weighing 11.5 lbs. (5.2 kg) was used. Moreover, use of TEE for both hemodynamic assessment and proper REBOA positioning obviates any exposure to radiation. In situations where REBOA has been employed for life-threatening hemorrhage, TEE has been used to confirm guidewire placement in the descending aorta [22]. Malpositioned REBOA, including inappropriate advancement into the ascending aorta, has potentially catastrophic consequences, including arrhythmia, carotid dissection, and coronary vasospasm [21]. Use of basic TEE is feasible with the advent of smaller, portable machines and probes, thus limiting radiation exposure and reducing the “footprint” associated with fluoroscopy.

There are several limitations to this work. Although the basic TEE exam requires less training and is easier to perform, advanced measurements, including functional measurement of stroke volume, cardiac output, stroke volume variation, and regional myocardial wall motion would likely be helpful to measure in future studies. Advanced calculations were obtained randomly in each experimental group for this study, but regular measurement of these parameters requires a more thorough exam performed by a practitioner with advanced TEE training. Basic TEE measurements were obtained prior to experimental hemorrhage and after REBOA inflation post-hemorrhage. Additional TEE exams conducted at regular intervals might have been more likely to reveal hemodynamic changes.

Basic TEE is feasible in porcine hemorrhagic shock models involving REBOA. This method can be performed with relative ease and may assist with early detection of hypovolemia and confirmation of precise proximal REBOA deployment. Basic TEE requires less training than advanced TEE and may be employed by laboratory investigators and practitioners across a wide spectrum of experimental and clinical settings.