An integral part of the care of end-stage renal disease (ESRD) patients is the time during which an attending nephrologist is at the bedside. During these time periods, an attentive clinician can solve acute and long-term problems by careful history taking and physical examination. The physical examination usually includes inspection, palpation, percussion, and auscultation. However, the traditional physical examination is known to be of limited value to detect common clinical problems such as fluid overload [1–3]. To identify immediate and long-term threats, the right tool in the right hands might be a decisive factor. Following the miniaturization of ultrasound devices, insonation has been proposed as the fifth pillar of physical examination [4▪▪]. Point-of-care ultrasound (POCUS) is now commonly used in emergency medicine, anesthesiology, and critical care medicine. The guiding principle is that a focused evaluation at the bedside performed by a trained clinician can help answer a clinical question. The goal of this approach is not to replace traditional diagnostic ultrasound performed by specialists, but to enable clinicians to take informed decisions based on objective findings in a timely manner. An ultrasound assessment can also be repeated to monitor the response following an intervention. This rationale has recently gained acceptance in fields which traditionally favored detailed diagnostic ultrasound such as cardiology [4▪▪]. Nevertheless, at the present time, more than 80% of American nephrology fellows do not receive POCUS training . The objective of this short review is to describe the applications of POCUS in ESRD patients. We will briefly review the recent developments concerning the use of lung ultrasound in dialysis patients. Additionally, we will explore the role of cardiac, abdominal, and vascular access ultrasound by giving clinical examples on how POCUS could contribute to facilitate the diagnosis or management of problems in ESRD patients.
LUNG ULTRASOUND IN END-STAGE RENAL DISEASE PATIENTS
Air represents a barrier to ultrasounds compared to solid tissues or liquids. Consequently, the normal aerated lung parenchyma is not seen when performing ultrasound. However, pathological processes can be diagnosed using ultrasound by detecting abnormal images or artifacts. Pulmonary congestion, represented by extra-vascular lung water (EVLW), can be measured semi-quantitatively by detecting an artifact named B-line or comet-tail. This artifact is caused by the reverberations of sound between aerated and fluid-filled lung parenchyma adjacent to the visceral pleura . An example is shown in Fig. 1. This “artifact" marker can be seen in patients with cardiogenic lung edema, acute respiratory distress syndrome (ARDS), or other interstitial lung disease such as pulmonary fibrosis . However, this artifact will be absent in other causes of dyspnea such as chronic obstructive pulmonary disorder (COPD) or asthma. As such, it has been successfully used in the emergency department to differentiate between acute COPD exacerbation and lung edema in the acutely dyspneic patient . In critically ill patients, the quantification of B-lines was demonstrated to be accurate for EVLW compared with wedge pressure, chest radiography or quantified using the indicator dilution method .
Observational studies have demonstrated that pulmonary B-lines are detected in ESRD patients even in the absence of overt symptoms such as dyspnea or peripheral edema [10,11]. Moreover, B-line count decreases during hemodialysis proportionally to fluid removal [12,13▪]. The adverse effects of chronic pulmonary congestion measured by B-line assessment have been investigated in ESRD patients. In one study, the amount of detected B-lines was associated with impairment in physical functioning  and moderate (>15 B-lines) to severe (>60 B-lines) pulmonary congestion was associated with an increased mortality risk in two large prospective cohorts of patients [15,16]. However, in a subsequent study, adding this measurement to other commonly used prognostic factors and left ventricular mass index measured by echocardiography did not improve the prediction of mortality .
Lung ultrasound may help clinicians in a variety of clinical contexts. In a dyspneic hemodialysis patient arriving for his treatment, assessing pulmonary B-lines may help to differentiate pulmonary edema from an exacerbation of COPD, leading to a correct diagnosis and appropriate intervention in a timely manner . Identifying patients with a high bilateral B-line burden may also prevent short-term hospitalizations for pulmonary edema. In a recent observational study by our group, patients with B-lines present in more than 20% of lung regions after hemodialysis had a 50% risk of hospitalization for pulmonary edema in the following year [13▪]. An asymmetric pattern of B-lines suggests the presence of a lung consolidation adjacent to the visceral pleura which can sometimes be seen when the parenchyma is completely filled with fluid (as shown in Fig. 1d). Pneumonia can be challenging to diagnose in dialysis patients and lung ultrasound is a useful adjunct for the clinician . Additionally, the examination may reveal pleural effusion which are due to overhydration in more than 60% of cases but may also be the hallmark of uremic pleuritis . An example of a large pleural effusion is presented in Fig. 1e. Finally, in the patient with dyspnea after dialysis catheter installation, the absence of pleural motion or lung sliding is a rapid and reliable method to detect a pneumothorax . This might be relevant to diagnose in dyspneic patients following insertion of a dialysis catheter in the jugular or subclavian area.
Whether the reduction of pulmonary B-lines should be considered a treatment target to improve the prognosis of hemodialysis patients is currently under investigation. A multicenter randomized controlled trial (LUST study) is underway, aiming to reduce the total number of B-lines to less than 15 by progressively increasing fluid removal in patients at high risk for cardiovascular events. In a related open-label randomized controlled trial in which low-risk patients of two hemodialysis centers were included, this intervention did not result in a reduction in cardiovascular events or mortality over a 2-year period (22.8% in the intervention group vs. 20.5% in the control group, P = 0.75) [22▪▪]. Of note, this study was underpowered for the primary endpoint (death or first cardiovascular event). However, the nonsignificant increase in events in the intervention group suggests that targeting a B-line score of less than 15 by reducing target weight may not be valid strategy to improve outcomes in low-risk hemodialysis patients. Pending the results of the LUST trial, clinicians should be aware that the use of pulmonary ultrasound to guide precise target weight prescription in the long term has not been demonstrated to improve outcomes, as for other technologies such as bioimpedance or blood volume monitoring [23▪,24].
INFERIOR VENA CAVA ULTRASOUND IN END-STAGE RENAL DISEASE PATIENTS PATIENTS
Imaging of the inferior vena cava (IVC) using POCUS can be performed reliably with basic training and equipment . This assessment has been studied to estimate central venous pressure (CVP) and to predict fluid responsiveness in critically ill patients. Although IVC diameter measurements are not able to precisely estimate CVP values, they can discriminate between normal/low CVP and high CVP values [26,27]. As shown in Fig. 2a and b, an IVC diameter of >21 mm with a variation of <50% with sudden inspiration  or <20% during normal breathing  reflects a high CVP (10–20 mmHg). In opposition, an IVC diameter of ≤21 mm and respiratory variations >20% are associated with a normal CVP (0–5 mmHg) (Fig. 2c and d) . Additionally, as the CVP increases, the IVC changes from an oval form to a spherical form. A ratio >0.69 between the anteroposterior and the lateral diameter is associated with a high CVP (≥10 mmHg) [29▪].
In ESRD patients, measurements of the IVC diameter and collapsibility have been studied as a tool to help target weight prescription in observational studies. In a sub-study of the Dry-weight Reduction in hypertensive hemodialysis Patients (DRIP) trial , IVC ultrasound was performed 30 to 60 min after dialysis . In this study, IVC diameter decreased in the intervention group subjected to incremental reduction in target weight. However, no relationship was found between IVC and blood pressure measurements during the intervention. In a recent study, IVC and bioimpedance measurements were performed before dialysis in 16 pediatric patients. IVC measurements did not correlate with extracellular fluid volume . Only one study reported IVC ultrasound in peritoneal dialysis patients. In this population, a correlation was found between IVC measurements and plasma atrial natriuretic peptide . In summary, the role of IVC ultrasound in target weight prescription in ESRD patients remains unclear.
In specific situations, IVC ultrasound may be useful to the attending physician. In patients with significant diuresis, an IVC value suggestive of a normal CVP in conjunction with the absence of pulmonary B-lines before dialysis may identify patients for whom fluid removal is unnecessary and might lead to repeated hypotensions which are known to be deleterious for residual kidney function . Similarly, when caring for an ESRD patient hospitalized for an acute condition, the prescription of fluid removal can be challenging for the clinician and IVC ultrasound could be useful to estimate CVP. In a recent observational study in 59 hospitalized hemodialysis patients, IVC measurements were accurate to predict high or low CVP but not adverse events during dialysis. The sample size was underpowered to detect a difference in the rate of intradialytic hypotension [35▪]. Finally, IVC ultrasound may be used in case of prolonged hemodynamic instability during hemodialysis where the finding of a dilated/fixed IVC should raise the suspicion of cardiogenic shock or pericardial tamponade . This finding should prompt the clinician to perform a focused cardiac assessment as described in the next section, whereas a compliant/collapsed IVC suggests hypovolemic or distributive shock such as sepsis or anaphylaxis. The rapid identification of the mechanism of shock is of paramount importance as the time to identification and intervention is a major factor associated with improved outcomes [37,38].
FOCUSED CARDIAC ULTRASOUND IN END-STAGE RENAL DISEASE PATIENTS
Although performing detailed cardiac ultrasound requires advanced training, a focused cardiac ultrasound can be performed at the bedside in the context of hemodynamic instability to quickly detect life-threatening conditions. An examination using three basic views presented in Fig. 3 allows a rapid evaluation of the biventricular function and pericardial space. Consequently, the trained clinician can diagnose clinically significant pericardial effusions, acute left ventricular systolic dysfunction, and right ventricular dilatation.
With specialized training, it is also possible to detect dynamic abnormalities during dialysis which would not be detected during elective diagnostic echocardiography in the radiology department. Fluid removal may induce transient episodes of left ventricular outflow tract obstruction and mitral valve regurgitation by a systolic anterior motion of the mitral valve during the cardiac cycle [39–41]. Myocardial stunning, defined as new abnormal wall motion during or after dialysis, may identify patients with coronary artery disease suffering from repeated episodes of myocardial ischemia because of increased myocardial demands and decreased cardiac output during dialysis [42,43]. Additionally, another potentially useful application would be to monitor change in left atrial volume, a simple parameter strongly associated with cardiovascular risk in ESRD patients. Left atrial volume may be a better indicator of the clinical impact of concentric myocardial hypertrophy than the left ventricular mass index  and might also be useful in identifying patients with progressive left ventricular diastolic dysfunction and worsening mitral valvular disease .
ABDOMINAL ULTRASOUND IN END-STAGE RENAL DISEASE PATIENTS
The traditional applications of abdominal POCUS are multiple and out of scope of this review. In the nephrology clinic, renal and bladder ultrasound can be used to rule out urinary obstruction and should be the first step in the setting of a sudden reduction of residual urine output. Bladder ultrasound is a simple assessment and can reveal a full bladder suggestive of lower urinary tract obstruction in the setting of an acute reduction in urine output. Hydronephrosis can also be detected with basic training in renal ultrasound.
In the setting of varying degrees of right ventricular dysfunction and fluid overload, the impact of venous hypertension can be assessed using Doppler ultrasound of the liver vessels. When the CVP increases, the compliance of the IVC decreases and variation of right atrial pressure during the cardiac cycle can be transmitted to the portal circulation. This results in abnormal velocity variations during the cardiac cycle. A variation of blood flow velocity in the portal vein during the cardiac cycle superior to 50% is abnormal. This is often called portal pulsatile flow. Portal flow pulsatility has been associated with abnormal bilirubin in chronic heart failure patients suggestive of impairment of liver function because of venous congestion . Similarly, other signs of abdominal organ congestion such as bowel edema can be detected by ultrasound and are associated with inflammation and cachexia in congestive heart failure patients . Given the relationship between fluid overload, inflammation and adverse outcomes in ESRD patients, the effect of bowel congestion should be further investigated [48,49▪,50].
ULTRASOUND FOR VASCULAR ACCESS
Although the installation of permanent venous access is usually performed by radiologists in a controlled setting, temporary dialysis catheters can be installed by the nephrologist when rapid access to an interventional radiologist is not an option. Several trials have shown that the use of real-time ultrasound guidance for the installation of dialysis catheters reduces failure rate and complications . Using ultrasound is enabling the clinician to evaluate the patency of the vein and guide the needle to avoid arterial puncture or pneumothorax, as presented in Fig. 4. Ultrasound guidance is recommended in anesthesiology , intensive care guidelines [53▪], and by the Kidney Disease: Improving Global Outcomes (KDIGO) guidelines on acute kidney injury . Given the high grade evidence from randomized controlled trials, the use of real-time ultrasound guidance for dialysis catheter installation should be mandatory.
Ultrasound assessment has been used for the evaluation of arteriovenous fistula and grafts. Three potential applications can be identified: planning for fistula creation, assessing the maturation of the fistula, and identifying problems once used. The routine evaluation of native artery and veins before fistula creation has been studied in multiple trials and summarized in two meta-analyses demonstrating that this was not associated with improved fistula outcomes, except for a reduction in immediate failure rate [55,56]. A detailed evaluation is usually done by experienced radiologists, but this specialized skill may be acquired by an interventional nephrologist performing nonsurgical arteriovenous access creation. For the nephrologist involved in the care of dialysis patients, the decision to begin using a fistula and the troubleshooting of problems during the use of fistula are common occurrences for which POCUS is useful. Using a linear probe, the diameter, distance from the skin, and blood velocity can be assessed with basic training. The Kidney Disease Outcomes Quality Initiative (KDOQI) guidelines on vascular access recommended that fistula maturation could be evaluated by the rule of six “a flow greater than 600 ml/min, a diameter at least 0.6 cm, no more than 0.6 cm deep, and discernible margins” . All those features can be easily assessed in a matter of minutes using POCUS at the bedside and reassessed over time to determine the optimal timing to begin using the access. Additionally, POCUS can be used to reassess the access characteristics in the setting of dysfunction or asymptomatic reduction of blood flow though the access. Although preemptive correction of arteriovenous access stenosis is currently not associated with a significant reduction of access loss , a better knowledge of the vascular access anatomy may increase awareness and perhaps lead to a lower threshold for intervention in some patients. In the setting of an acute dysfunction, POCUS can quickly identify thrombosis as shown in Fig. 5.
The applications of POCUS in ESRD are multiple (Table 1). Basic POCUS training including IVC ultrasound , pulmonary ultrasound , and limited cardiac ultrasound  can be learned over a short period of time resulting in similar skill compared to specialized training. Moreover, training can be provided online with excellent results . Although lung ultrasound has generated interest in the nephrology community, the potential impact of the widespread adoption of POCUS in the care of nephrology patients goes beyond this specific assessment. It may be challenging to prove that training nephrologists in POCUS will result in better outcomes in ESRD patients. However, as more clinicians diagnose life-threatening conditions with this tool, it may become impossible to convince them that their physical examination is complete without insonation. With basic curriculum now integrating POCUS in undergraduates [62▪], internal medicine [63▪], and nephrology training [64▪▪], a famous quote by Victor Hugo comes to mind: “You can resist an invading army; you cannot resist an idea whose time has come.”
We sincerely thank Denis Babin (Research Assistant) for his help in manuscript preparation.
Financial support and sponsorship
W.B.-S. receives salary support from Fonds de Recherche du Québec en Santé (FRQS). A.D. is supported by the Richard Kaufman Endowment Fund in Anesthesia and Critical Care and the Montreal Heart Institute Foundation.
Conflicts of interest
Dr André Denault is on the Speaker bureau for CAE Healthcare.
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Papers of particular interest, published within the annual period of review, have been highlighted as:
- ▪ of special interest
- ▪▪ of outstanding interest
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