Perioperative Point‐of‐Care Ultrasound Utilization in Abdominal Organ Transplantation. Part I: Preoperative and Intraoperative Care

ABSTRACT

In this Society for the Advancement of Transplant Anesthesia (SATA) white paper, experts in abdominal transplant anesthesia and critical care reviewed the current literature and practice behaviors to create a comprehensive review of the utilization of point‐of‐care ultrasound (PoCUS) in abdominal organ transplantation (AOT) and to provide evidenced‐based recommendations for clinicians to utilize perioperative PoCUS to improve patient outcomes in real time. Organized by phase of care–preoperative, intraoperative, and postoperative–this paper includes a discussion of transthoracic, pulmonary, gastric, and transesophageal echocardiography. Part I of this paper focuses on preoperative and intraoperative PoCUS while the upcoming Part II focuses on utilizing PoCUS in the immediate postoperative and intensive care setting to guide fluid management, identify venous congestion, identify causes of shock, and estimate hemodynamics in AOT patients.

Abbreviations

A4C

apical four chamber

AOT

abdominal organ transplantation

AV

aortic valve

BMI

body mass index

CF

color flow

CSA

cross‐sectional area

CVP

central venous pressure

CW

continuous wave

EPSS

end point septal separation

FAC

fractional area change

ICU

intensive care unit

IVC

inferior vena cava

LA

left atrium

LV

left ventricle

LVEDA

left ventricular end‐diastolic area

LVEDD

left ventricular end‐diastolic diameter

LVEF

left ventricular ejection fraction

LVOT

left‐ventricular outflow tract

MAPSE

mitral annular plane systolic excursion

ME 4C

midesophageal four chamber

ME LAX

midesophageal long axis

ME RV inflow‐outflow

midesophageal right ventricular inflow‐outflow

MRI

magnetic resonance imaging

MV

mitral valve

NPO

nil per os

OR

operating room

PA

pulmonary artery

PASP

pulmonary artery systolic pressure

PLAX

parasternal long axis

PoCUS

point‐of‐care ultrasound

PSAX

parasternal mid‐papillary short axis

PV

pulmonic valve

PW

pulse wave

RA

right atrium

RAP

right atrial pressure

RLD

right lateral decubitus

RV

right ventricle

RVEF

right ventricular ejection fraction

RVFAC

right ventricular fractional area change

RVOT

right‐ventricular outflow tract

RWMA

regional wall motion abnormality

SAM

systolic anterior motion of the mitral valve

SATA

Society for the Advancement of Transplant Anesthesia

TAPSE

tricuspid annular plane systolic excursion

TEE

transesophageal echocardiography

TG midpapillary SAX

transgastric midpapillary short axis

TR

tricuspid regurgitation

TTE

transthoracic echocardiography

TV

tricuspid valve

V _TR

tricuspid regurgitation velocity

1. Introduction

All patients undergoing abdominal organ transplantation (AOT)–liver, renal, pancreas, and intestinal transplantation–have end‐stage or impending end‐stage disease in one or more organs. Although these patients typically undergo a comprehensive workup before being listed for an AOT, months may pass between the initial workup and the allocation of an organ–leaving the transplant anesthesiologist with an incomplete understanding of the patient's current fitness. As these procedures are commonly unscheduled, yet time sensitive, patients undergoing AOTs often present with unclear nil per os (NPO), preload, and ascites and pleural effusion statuses–all of which may also affect the patient's readiness to proceed to the operating room (OR). As a result of physiologic derangement from end‐stage organ disease and the technical difficulty of the surgical procedures, these patients can suffer from large‐volume blood loss, vasoplegia, and decreases in cardiac function–all leading to intraoperative and postoperative hemodynamic instability.

Point‐of‐care ultrasound (PoCUS) is an emerging discipline where clinicians utilize ultrasound machines to answer specific clinical questions, not to complete comprehensive examinations of a specific organ. By directly ruling‐in or ruling‐out pathologies at the bedside, the clinician is able to make a more informed and timely decision in solving the underlying cause(s) of the patient's condition.

With the decreased cost and increased portability of modern ultrasound machines, the utilization of PoCUS to address clinical questions has significantly increased. Many papers exist that review PoCUS examinations of a specific organ system or patient population. To date, however, no comprehensive review of the utility of PoCUS examinations in AOT exists.

In this Society for the Advancement of Transplant Anesthesia (SATA) white paper, experts in abdominal transplant anesthesia and critical care medicine reviewed the current literature and practice behaviors to create a comprehensive review of the utilization of PoCUS in AOT and to provide evidenced‐based recommendations for clinicians to utilize perioperative PoCUS to improve patient outcomes in real time. Organized by phase of care–preoperative, intraoperative, and postoperative–this paper includes discussion of transthoracic, pulmonary, gastric, and transesophageal echocardiography (TEE). Part I of this paper focuses on preoperative and intraoperative PoCUS while the upcoming Part II focuses on utilizing PoCUS in the immediate postoperative and intensive care settings to guide fluid management, identify venous congestion, identify causes of shock, and estimate hemodynamics in AOT patients.

2. Preoperative Point‐of‐Care Ultrasound

2.1. Cardiac: Transthoracic Echocardiography (TTE)

In the preoperative period, TTE can be utilized to ascertain the cardiac functional status, volume status, and systemic vascular resistance [1].

Parasternal mid‐papillary short axis (PSAX) view helps to evaluate cardiac contractility and provides visualization of the left ventricle (LV), right ventricle (RV), as well as the interventricular septum (Figure 1A). This view is useful to identify regional wall motion anomalies (RWMAs), as all the segments of the LV are visible. The presence of a D‐shaped LV or a flattened interventricular septum indicates RV volume/pressure overload and reflects a poor prognosis. Fractional area change (FAC) of the LV can be calculated in PSAX view (Table 1). LVFAC correlates with left ventricular ejection fraction (LVEF) and normal value of FAC is 35%–65% [2]. LVFAC less than 20% reflects severe LV systolic dysfunction.

FIGURE 1.

Basic transthoracic echocardiography views.

TABLE 1.

Selected point‐of‐care ultrasound measurements obtainable via transthoracic echocardiography.

TTE View	PoCUS measurement and formula	Reference range
PSAX	LVFAC = (end diastolic LV area – end systolic LV area)/end diastolic LV area × 100	35%–65%
	LVEDD = distance between endocardium of the interventricular septum and free wall at end diastole	3.5–6.5 cm
	LVEDA = LV area measured at end‐diastole	8–14 cm2
PLAX	EPSS = distance from the tip of anterior mitral leaflet to the endocardium of the interventricular septum during diastole	<6 mm
A4C	RVFAC = (end diastolic RV area – end systolic RV area)/end diastolic RV area × 100	>35%
	PASP = 4 × [V TR (m/s)]2 + RAP (mm Hg)	<35 mm Hg
	MAPSE = systolic excursion of mitral annular plane evaluated in long axis in M mode	>1.3 cm
	TAPSE = systolic excursion of tricuspid annular plane evaluated in long axis in M mode	>1.6 cm

Measuring the left ventricular end‐diastolic diameter (LVEDD) in PSAX view gives us a good estimate of volume status; a value less than 3.5 cm strongly suggests hypovolemia. Normal range for LVEDD is 3.5–5.6 cm. A left ventricular end‐diastolic area (LVEDA) less than 8 cm² also suggests hypovolemia, while an area greater than 14 cm² indicates poor cardiac contractility. LVEDA is a good surrogate marker of preload [3]. The presence of increased contractility and normal left ventricular end‐diastolic diameter signifies low systemic vascular resistance. Parasternal short axis aortic valve (AV) view is useful to visualize the tricuspid valve and the pulmonic valve (PV).

The parasternal long axis (PLAX) view (Figure 1B) can be used to calculate end point septal separation (EPSS). EPSS correlates with left ventricular function [4]. EPSS is the distance from the tip of an anterior mitral leaflet to the endocardium of the interventricular septum during diastole. A value higher than 17 mm signifies severely decreased LVEF, and a value between 12–17 mm reflects moderately decreased LVEF. A normal LV contractility is reflected by EPSS less than 6 mm. The left atrial (LA) and RV size can also be measured in this view. An LA diameter greater than 4 cm signifies LA enlargement, while an RV diameter greater than 3.3 cm signifies a dilated RV.

The apical four chamber (A4C) view (Figure 1C) is useful to measure the LVEF and right ventricular ejection fraction (RVEF). A normal LVEF ranges between 55% and 69%. There are some limitations to accurate assessment of LV contractility with this method including left ventricular foreshortening and interobserver variability. Measurement of mitral annular plane systolic excursion (MAPSE) also provides a qualitative estimate of contractility of the LV, where a value less than 1.3 cm signifies poor contractility. Right ventricular fractional area change (RVFAC) is used as a measure of RVEF (Table 1). A normal RVFAC is greater than 35%. RVFAC correlates with cardiac magnetic resonance imaging (MRI) derived RVEF [5].

Tricuspid annular plane systolic excursion (TAPSE) is used to qualitatively assess RV systolic function [6]. TAPSE greater than 16 mm signifies a normal RV systolic function. The Doppler cursor is sometimes not perfectly aligned with tricuspid annulus for correct measurement of TAPSE, leading to inaccurate results. An RV internal diameter greater than 2/3rd of LV internal diameter signifies RV dysfunction.

Pulmonary artery systolic pressure (PASP) can be estimated in the A4C view using continuous wave (CW) Doppler to interrogate the tricuspid regurgitation (TR) jet velocity and to measure peak systolic TR velocity (V _TR, Table 1). Central venous pressure (CVP) can be measured via a central venous catheter and used as a surrogate of right atrial pressure (RAP). The calculation of PASP can be particularly helpful in determining the severity of portopulmonary hypertension and, therefore, the need for additional monitoring or RV support intraoperatively. Color flow (CF), pulse wave (PW), and CW Doppler can be used to assess for mitral and tricuspid valvular regurgitation and stenosis. Diastolic function of the LV is assessed by Doppler PW analysis of mitral valve (MV) inflow and pulmonary vein flow as well as tissue Doppler analysis of lateral mitral annulus [7].

The subcostal 4‐chamber view (Figure 1D) can be utilized to visualize pericardial effusions and RWMA. From the subcostal 4 chamber view, the probe is turned counterclockwise by 90° to obtain the inferior vena cava (IVC) view. It is vital to see the right atrial–IVC junction. IVC diameter is measured 1–2 cm from the cavo‐atrial junction. An IVC diameter of less than 1.3 cm warrants fluid administration [8].

Although not typically performed outside of rescue scenarios where unexplained intraoperative hypotension is encountered, PoCUS TTE examination may be completed intraoperatively utilizing the same views as described in section 2.1. If the needed window is in the surgical field, a phased array probe with a sterile probe cover may be provided to the surgeon. Guidance should then be provided to assist the surgeon in obtaining the needed view.

2.2. Pulmonary Ultrasonography

In brightness (B) mode, an ultrasound mode that displays two‐dimensional imaging of tissue in grayscale, healthy lung (Figure 2A) is represented by the presence of lung sliding (back and forth movement of pleura‐ also referred to as pleural sliding) and the presence of A lines, which are lines parallel to the pleural line indicative of reverberation artifacts of the pleura. In motion (M) mode, a motion versus time display of B mode imaging along a chosen line, a healthy lung exhibits a seashore sign, the presence of horizontal lines above the pleural line and granular pattern below the pleural line (Figure 2A).

FIGURE 2.

Lung ultrasound examples.

Blue protocol helps in the detection of various lung pathologies [9, 10]. Lung ultrasound can help to detect the presence of a pleural effusion or consolidation. Pleural effusion appears as a dark hypo‐echoic structure when the probe is placed at the dependent lung zones (Figure 2B). In M mode, there is a decrease in the apparent thickness of pleural effusion during inspiration (sinusoidal sign). Large pleural effusions can be drained perioperatively under ultrasound guidance.

The presence of air bronchograms that move with respiration reflects the early phase of consolidation (Figure 2C). As the consolidation advances, the presence of B lines in one part of the lung with absent lung sliding, as well as the presence of A lines in other parts of the lung can be seen. As consolidation increases further, the shred sign or C profile is present. The consolidated lung tissue is represented by a subpleural hypo‐echoic region with an irregular deep border adjacent to the healthy lung. Lobar consolidation is represented by hepatization of the lung tissue‐ the lung tissue appears similar to liver tissue.

Pulmonary edema can be diagnosed by the presence of B lines in all the zones of both the lungs. B lines are vertical, laser‐like, hyper‐echoic lines that extend from the pleural line to the bottom of the ultrasound screen. B lines erase the A lines. Counting the number of B lines helps in quantifying the pulmonary edema [10]. This is a useful tool to assess the effectiveness of dialysis in patients with underlying hepato‐renal syndrome in potential liver transplant recipients and in end‐stage renal disease in potential renal transplant recipients. As B lines disappear after effective dialysis, pulmonary ultrasonography can be utilized to determine whether additional preoperative dialysis treatments are warranted before AOT.

A high‐frequency linear probe is placed in the upper zones of the lung to detect a pneumothorax. In B mode, lung sliding is absent and A lines are present in the area of pneumothorax. In M mode, there is an absence of a normal granular pattern below the pleural line. Instead, there are many horizontal lines (stratosphere or barcode sign, Figure 2D) [10]. This examination is of particular importance in patients undergoing intestinal transplantation. More than 50% of these patients present for transplantation with at least one thrombosed large caliper vessel due to the prior administration of total parenteral nutrition–with the internal jugular veins being the most commonly affected [11]; therefore, central venous access through the subclavian vein is more commonly utilized than in other AOTs. Although commonly regarded as safe, selecting this location of access has been shown to be up to three times more likely to cause a pneumothorax or hemothorax requiring a chest tube compared to the internal jugular vein [12, 13]. Numerous studies have shown that pulmonary PoCUS has a higher sensitivity and similar specificity for diagnosing pneumothorax compared to a portable chest x‐ray [14, 15, 16].

2.3. Gastric Ultrasonography

The incidence of gastric aspiration varies amongst patient populations and surgical procedures but is reported to be anywhere from 0.1% to 19% [17]. Aspiration pneumonia because of pulmonary aspiration of gastric contents usually carries with it significant morbidity and mortality risk [18]. Aspiration of gastric contents accounts for about 5% of malpractice closed claims between the years of 2000–2014 with patient mortality of greater than 50% [19]. With the expansion of point‐of‐care ultrasound application in clinical practice, ultrasonography of the stomach has been added to the armamentarium of the perioperative physicians to assist with decision making, in addition to the routine patient interview and fasting information.

Gastric ultrasound can be deployed to assess the quality and quantity of contents before induction of anesthesia, which in turn can help guide the anesthesiologist's decision to proceed with standard induction or a rapid sequence intubation. There is no consensus on what volume of gastric secretion is considered safe from an aspiration risk standpoint, but the absence of solid food and clear volumes of up to 1.5 mL/kg are considered normal in fasting patients. A quick scan can help to determine the NPO status of the preoperative patients with risk factors for a full stomach despite appropriate fasting times. Recommended fasting times are reported by the American Society of Anesthesiologists for use in elective procedures; however, these have not been validated in patients with gastric motility issues, tense ascites, and emergent procedures. Patients undergoing liver transplantations who have significant ascites and patients undergoing pancreatic transplantations who have diabetic gastroparesis are two of the high‐risk AOT patient populations for having retained gastric contents [20]. Before the use of gastric ultrasound, the decision of induction technique varied significantly based on patient disease severity but now a quick scan can be used to assess both the quality and the volume of the stomach contents.

To perform a gastric ultrasound examination, the patient should be positioned in the supine position and/or the right lateral decubitus (RLD) position to obtain the optimum view to assess the gastric antrum [21]. RLD position is the preferred position due to gravity‐aided collection of gastric volume in the antrum, but it can be hard to achieve in patients who are moribund and/or in the intensive care unit (ICU) with mechanical ventilation. Low‐frequency curvilinear probe in a cephalo‐caudal orientation along the midline of the abdomen wall is used to obtain the standard view. The probe can be moved medially or laterally to optimize the view. The view preferably should include the view of the following structures: liver, gastric antrum, pancreas, superior mesenteric artery, and aorta (Figure 3).

FIGURE 3.

Gastric ultrasound examples. A = gastric antrum; A_O = aorta; IVC = inferior vena cava; L = liver; P = pancreas; SMA = superior mesenteric artery. Adapted from the British Journal of Anesthesia, 113(1), Putte and Perlas, Ultrasound Assessment of Gastric Content and Volume, 12, Copyright (2014), with permission from Elsevier.

The gastric antrum can be identified as the circular structure in cross‐sectional view with hyperechoic mucosal lining typically found posterior to the left lobe of the liver. Aortic pulsations can be used to identify the abdominal aorta in its long axis view which runs posterior to the gastric antrum. If the curvilinear probe is moved more laterally toward the pylorus, the IVC can be seen in the long axis. It can be differentiated easily from the aorta due to its thin walls, proximity to the liver tissue, and absence of pulsation. For purposes of assessing gastric content and volume, it is important to visualize the antrum and not the pylorus as the pylorus given its thicker wall and smaller diameter can lead to under‐estimation of gastric volume, and most mathematical models used to estimate volume are based on sonography assessment of the antrum. The pancreas is usually visualized as a hyperechoic structure posterior to the antrum and anterior to the superior mesenteric artery.

In an appropriately fasting patient, there should be no to minimal fluid visualized in the gastric antrum (Figure 3A). Gastric secretions and clear liquids will have the appearance of clear anechoic or hypoechoic fluid with no visible particulate matter (Figure 3B). Solid food is usually suggested by either particulate hyperechoic densities in the clear fluid, “starry sky” pattern, or with worsening view of the gastric antrum with the posterior wall of the stomach, and posterior structures like the pancreas and becoming difficult to visualize (Figure 3C). This appearance, seen with the prominent anterior wall of the antrum, distension of the antrum, and acoustic shadowing, is referred to as the “frosted glass or ground glass” pattern [22].

The volume of gastric content can be determined either qualitatively or quantitatively. When assessing volume from a qualitative perspective, the most reliable system is current literature is the Perla's three‐point grading system: Grade 0, no stomach contents visible in supine or RLD positions; Grade 1, no stomach contents visible in supine position but visible in the RLD position; and Grade 2, gastric fluid in both positions [23]. Grade 0 corresponds to a completely empty stomach, Grade 1 corresponds to negligible fluid volumes of <1.5 mL/kg, and Grade 2 corresponds to clinically significant >1.5 mL/kg volumes.

There are multiple mathematical models that have been proposed to quantitatively calculate the volume of gastric content [24, 25, 26]. Most of these models involve the use of cross‐sectional area (CSA) calculations to estimate the volume of gastric content. The CSA is usually calculated in the RLD position using both anteroposterior dimensions and craniocaudal dimensions of the gastric antrum measuring from serosa to serosa. The various models use different patient populations, varying among age groups, pregnancy status, and body mass index (BMI). Most of these are feasibility trials with small sample sizes, and there is a need for more robust studies in the future to improve the diagnostic accuracy of gastric ultrasound for assessing volume.

Ultimately, the goal of gastric ultrasonography is to provide quick assessment of content qualitatively and quantitatively to aid with preinduction decision making for the anesthesiologist and attempting to reduce the risk of aspiration events for our patients. Qualitative assessment itself has been shown to accurately identify patients with gastric volumes of more than 1.5 mL/kg and at high risk for aspiration with induction of anesthesia.

3. Intraoperative Point‐of‐Care Ultrasound

3.1. Cardiac: Transesophageal Echocardiography (TEE)

During liver transplantations, a significant number of anesthesiologists complete comprehensive TEE examinations, similar in nature to the examinations completed in cardiac procedures requiring cardiopulmonary bypass, as a matter of institutional protocol or norm. Numerous well‐written reviews exist on this topic which detail how to complete a comprehensive TEE examination [27, 28, 29].

Here, we will focus our attention on the TEE views which provide the most helpful diagnostic information to a transplant anesthesiologist–particularly one who does not routinely complete comprehensive examinations. Additionally, obtaining these views may be invaluable as a rescue measure in diagnosing the etiology of hypotension during the course of all AOTs. It should be noted that although care should be taken to avoid excessive force or probe manipulation as with every patient, obtaining TEE images in patients with liver failure is generally regarded as safe and not associated with increased‐risk compared to obtaining TEE images in patients undergoing cardiac surgery [30].

The midesophageal four chamber (ME 4C) view is a foundational view for the transplant anesthesiologist due to the variety and utility of the information that can be quickly obtained by utilizing it (Figure 4A). Obtained at a probe depth of approximately 30–35 cm with an omniplane angle of 10°–20°, the ME 4C demonstrates biatrial and biventricular size–which can provide information regarding volume status–as well as regional biventricular function [28, 29]. In this view, the inferoseptal and anterolateral walls of the LV and the lateral wall of the RV are visible. MV and tricuspid valve (TV) structure and function can also be evaluated as can less common pathology such as atrial or ventricular septal defects and pericardial effusions or tamponades.

FIGURE 4.

Basic transesophageal echocardiography views. Adapted from Journal of the American Society of Echocardiography, 26(5), Reeves et al., Basic Perioperative Transesophageal Echocardiography Examination: A Consensus Statement of the American Society of Echocardiography and the Society of Cardiovascular Anesthesiologists, 14, Copyright (2013), with permission from Elsevier.

The midesophageal long axis (ME LAX) view is located at a probe depth of approximately 30–35 cm, typically at the same depth as the ME 4C view, with an omniplane angle of 120°–140° [28] (Figure 4B). This view demonstrates the structure and function of the LA, MV, AV, left‐ventricular outflow tract (LVOT), and inferolateral and anteroseptal walls of the LV. Of particular importance to transplant anesthesiologists, this view provides a clear view to evaluate for the presence of a dynamic LVOT obstruction and systolic anterior motion of the mitral valve (SAM) [31].

The midesophageal right ventricular inflow‐outflow (ME RV inflow‐outflow) view is also obtained in the midesophageal depth with an omniplane angle of 50°–70° [28] (Figure 4C). This view provides for evaluation of the structure and function of the LA, right atrium (RA), TV, RV, PV, right‐ventricular outflow tract (RVOT), pulmonary artery (PA), and the AV. This view provides the transplant anesthesiologist the opportunity to evaluate for an intracardiac thrombus which is particularly important upon releasing caval cross‐clamps or upon rapid correction of coagulopathies in the liver [32] and intestinal transplantations [33, 34].

The transgastric midpapillary short axis (TG midpapillary SAX) view is obtained by advancing the probe from the midesophageal position into the stomach with an omniplane angle of 0°–20° until the posteromedial papillary muscle is visible [28, 29] (Figure 4D). The probe should then be anteflexed until the anterolateral papillary muscle is also well‐visualized. This view is unique in that it provides detailed imaging of the left ventricular myocardium that are perfused by the left anterior descending, right coronary, and circumflex coronary arteries allowing for the identification of regional wall motion abnormalities (RWMAs) suggestive of ischemia within their distributions. The TG midpapillary SAX view also provides information regarding global LV function and is the view is the most commonly utilized view for the estimation of preload and fluid responsiveness [35]. This is of particular importance during liver, intestinal, and renal transplantation. During liver and intestinal transplantation, it is imperative to adequately resuscitate the patient to compensate for significant blood loss, fluid shifts, and vasodilatory changes; however, it is also essential to not over resuscitate the patient and risk graft edema, anastomotic leak, abdominal compartment syndrome, or right ventricular failure [36]. During renal transplantation, maintaining euvolemia is essential to prevent delayed graft function, acute kidney injury, and pulmonary edema [37].

4. Conclusion

To date, a paper describing the utility of perioperative PoCUS in AOT has not been published. Guidelines describing transthoracic, pulmonary, gastric, and transesophageal PoCUS examinations in the preoperative and intraoperative setting are described here in order to promote increased utilization of perioperative PoCUS in the AOT patient population, to improve patient management and outcomes in real time, and to provide further education for our specialty. The upcoming Part II of this paper will focus on the utility of PoCUS for AOT in the postoperative care unit and ICU. Future research in this area is needed to investigate potential improvements in AOT morbidity and mortality with the inclusion of PoCUS and to determine whether specific PoCUS protocols can be implemented to optimize workflow and to decrease the likelihood of inducing a delay in the transplantation process.

Disclosures

The authors have nothing to report.

Conflicts of Interest

The authors declare no conflicts of interest.

Data Availability Statement

Data sharing is not applicable to this article, as no new data were created or analyzed in this study.