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    Gut and Liver is an international journal of gastroenterology, focusing on the gastrointestinal tract, liver, biliary tree, pancreas, motility, and neurogastroenterology. Gut atnd Liver delivers up-to-date, authoritative papers on both clinical and research-based topics in gastroenterology. The Journal publishes original articles, case reports, brief communications, letters to the editor and invited review articles in the field of gastroenterology. The Journal is operated by internationally renowned editorial boards and designed to provide a global opportunity to promote academic developments in the field of gastroenterology and hepatology. +MORE

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    Yong Chan Lee Professor of Medicine
    Director, Gastrointestinal Research Laboratory
    Veterans Affairs Medical Center, Univ. California San Francisco
    San Francisco, USA

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    Jong Pil Im Seoul National University College of Medicine, Seoul, Korea
    Robert S. Bresalier University of Texas M. D. Anderson Cancer Center, Houston, USA
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The Role of Endoscopic Ultrasound in Hepatology

Saleh A. Alqahtani1,2 , Floriane Ausloos3 , Ji Seok Park4 , Sunguk Jang4

1Division of Gastroenterology and Hepatology, Johns Hopkins University, Baltimore, MD, USA, 2Liver Transplant Centre, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia, 3Department of Gastroenterology and Hepatology, CHU Liège, Sart-Tilman, Liège, Belgium, and 4Department of Gastroenterology and Hepatology, Digestive Disease Institute, Cleveland Clinic, Cleveland, OH, USA

Correspondence to: Sunguk Jang
ORCID https://orcid.org/0000-0001-9837-0322
E-mail jangs@ccf.org

Received: February 22, 2022; Revised: May 19, 2022; Accepted: June 21, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Gut Liver.

Published online December 2, 2022

Copyright © Gut and Liver.

Endoscopic ultrasound (EUS) has been an indispensable and widely used diagnostic tool in several medical fields, including gastroenterology, cardiology, and urology, due to its diverse therapeutic and diagnostic applications. Many studies show that it is effective and safe in patients with liver conditions where conventional endoscopy or cross-sectional imaging are inefficient or when surgical interventions pose high risks. In this article, we present a review of the current literature for the different diagnostic and therapeutic applications of EUS in liver diseases and their complications and discuss the potential future application of artificial intelligence analysis of EUS.

Keywords: Endoscopic ultrasound, Liver diseases, Portal hypertension

Endoscopic ultrasound (EUS) has been an indispensable and widely used diagnostic tool since its initial description in the 1980s. Its diverse therapeutic and diagnostic applications have allowed for its use in various medical field, including gastroenterology, cardiology, and urology.1,2 In recent years, EUS has also proven effective and safe in patients with liver conditions where conventional endoscopy or cross-sectional imaging are inefficient and when surgical interventions pose high risks. Growing evidence shows that expanding therapeutic and diagnostic applications of EUS, especially in managing chronic hepatic diseases, outperform in accuracy compared to conventional imaging techniques, such as transabdominal ultrasound (US) and computer tomography (CT). More specifically, a major advantage of EUS is the proximity and ease of using the EUS transducer close to the liver and accurately identifying blood vessels and other intervening structures.3 Due to its superior performance and negligible adverse effects, EUS has been a highly preferred tool in identifying, characterizing, and staging primary and malignant liver tumors.4-6

Moreover, newly emerging echoendoscopes are provided with color, power and pulsed Doppler, enabling them to identify blood vessels and measure portal pressure in blood vessels.7,8 Combined EUS with real-time elastography (RTE) can effectively measure stiffness of the liver parenchyma and focal lesions.7 In addition, liver biopsy (LB) guided by EUS is safer with lower risks than the traditional percutaneous method.9

In this review, we discuss in detail previous and recent applications of EUS as a diagnostic and therapeutic tool in managing liver diseases and explain the potential future use of artificial intelligence analysis for EUS.

1. Focal liver lesions

EUS has the advantage of evaluating the appearance of focal liver lesions and taking samples of lesions for histological diagnosis. Focal liver lesions include benign (hepatic abscess, hepatic cyst, hemangioma, and hepatocellular adenoma) and malignant lesions (hepatocellular carcinoma [HCC], cholangiocarcinoma, and liver metastasis) and are traditionally diagnosed using conventional methods, such as transabdominal imaging and percutaneous tissue sampling. In most cases, focal liver lesions are incidentally found using cross-sectional imaging with US, CT, or magnetic resonance imaging in patients at high risk for hepatic malignancies.6,10 Understanding the nature of these lesions is extremely important for the prognosis of hepatic malignancies. However, conventional screening using US, CT, and magnetic resonance imaging has its limitations in accurately diagnosing the nature of these lesions, especially for smaller lesions (<10 mm).11,12 EUS outperforms in its diagnostic accuracy compared to these traditional modalities with the power to diagnose lesions smaller than 10 mm.6,13 In a prospective study in patients with gastrointestinal or pulmonary malignancies, EUS identified liver lesions with high accuracy in 14 patients compared to CT, which only detected three of the lesions.14 More studies have validated the superiority of EUS over CT by accurately detecting lesions <5 mm in diameter.15,16 In fact, one of these studies showed that EUS detected an additional 28% of hepatic lesions among 14 patients with a history of suspected hepatic malignancies previously detected by CT.15 Diagnostic accuracy of EUS and CT for detecting hepatic lesions were found to be 98% and 92%, respectively, with EUS significantly detecting a higher number of hepatic metastatic lesions compared to CT.16

Elastography is a noninvasive method using US waves to assess liver stiffness. It has a strong correlation with the degree of liver fibrosis demonstrated by LB. However, the technique is limited to people with ascites, narrow intercostal spaces, and body habitus.17 EUS elastography can overcome most of these limitations and has been described as a significant tool in identifying, differentiating, and characterizing malignant and benign hepatic focal lesions with a diagnostic accuracy, sensitivity, and specificity of 88.6%, 92.5%, and 88.8%, respectively.18-20 Malignant liver masses are stiffer than benign masses, and EUS elastography's ability to quantify the stiffness has rendered it a valuable tool in characterizing liver lesions.21

In addition, hepatic microvascular architecture can be better visualized using contrast agents. Contrast enhancement (CE) is widely used to improve the diagnostic performance of US and EUS. Contrast-enhanced-EUS (CE-EUS) is classified into CE-EUS with the Doppler method and CE-EUS with harmonic imaging, which allows improved detection and characterization of focal liver lesions.22 Like CE-US, CE-EUS can be used to detail different types of liver lesions through vascular enhancement patterns, with typical patterns including arterial hyperenhancement: (1) subsequent wash out in late-phase contrast in HCC; (2) rim-like enhancement and subsequent rapid washout in metastatic hepatic cancer; (3) with progressive, early, spoke-wheel arteries, unenhanced central scar in focal nodular hyperplasia, and peripheral nodular hyperenhancement; (4) with centripetal progressive fill-in hemangioma.23-25

Moreover, CE-US has been demonstrated to be a valuable tool to evaluate the effectiveness of HCC treatment with a sensitivity and accuracy of 95.6% and 96.2%, respectively, and to detect residual tumor with a sensitivity and accuracy of 76.2% and 77.7%, respectively.26 Given these observations, CE-EUS could be of potential value with superior accuracy in detecting deep liver lesions over CE-US.27 However, further studies are required to validate it.

In a retrospective analysis, Fujii-Lau et al.28 developed a EUS scoring system to distinguish between benign and malignant hepatic masses by analyzing data from patients who underwent EUS-fine needle aspiration (FNA) of solid hepatic masses. The derived and validated EUS criteria showed a high positive predictive value of 88% and could detect radiographically occult masses <5 mm. Moreover, the scoring system could enable endosonographers to make informed decisions to avoid unnecessary FNA interventions. Multicenter studies involving multiple endosonographers are required to further validate the scoring system. The algorithm is described in Fig. 1.

Figure 1.Scoring system based on sonographic criteria in distinguishing benign lesion from malignant lesion.

2. Liver cirrhosis

LB is the gold standard diagnostic tool for liver cirrhosis; however, its application is limited due to sampling errors, complications associated with it being an invasive procedure, inter-observer variability, and cost.29 Several noninvasive modalities, based on noninvasive fibrosis markers, such as transient elastography (TE), and RTE to measure liver stiffness, have been developed to overcome these limitations.30 Nonetheless, the performance to detect fibrosis is suboptimal as the transabdominal approach is limited in obese patients and individuals with ascites.29 In such scenarios, EUS-guided liver stiffness measurements are advantageous and can overcome barriers given the transducer's proximity to the liver, thereby accurately assessing liver fibrosis.31 Moreover, EUS RTE is more sensitive than transabdominal RTE in evaluating liver fibrosis because the signal passes through the thin gastric wall versus the abdominal wall in transabdominal RTE.32 Liver fibrosis index, calculated using EUS RTE images, significantly correlates with transabdominal imaging and can accurately stratify normal, fatty, and cirrhotic livers.32 Given these advantages, EUS RTE can be both an effective and time-efficient modality for assessing fibrosis in patients with liver diseases, especially when patients undergo upper endoscopy for variceal screening or other indications. Furthermore, additional information about liver parenchyma can be obtained all in one session.

Another study evaluating the diagnostic value of EUS, Fibroscan, and acoustic radiation force impulse to detect esophagogastric varices, liver stiffness measurement, and liver virtual touch tissue quantification, respectively, in patients with chronic viral liver disease, reported significantly higher detection rate for early-stage liver cirrhosis (Child-Pugh A grade) than chronic hepatitis. Moreover, the combination of these three modalities had a superior diagnostic value for early-stage liver cirrhosis.33 The regression model of EUS, Fibroscan, and acoustic radiation force impulse reported an area under the receiver operating characteristic curve (AUROC) of 0.947 with a sensitivity and specificity of 0.878 and 0.867, respectively.

These results suggest a promising role for EUS along with other modalities in early and accurate diagnosis of complications in early liver cirrhosis and may improve the diagnosis rate and decrease the misdiagnosis rate.

3. Portal hypertension

Cirrhosis can lead to portal hypertension (PHT), defined as a major hemodynamic shift due to increased pressure in the portal vein (PV), and correlates to complications, such as ascites, variceal bleeding, and encephalopathy.34 Thus, prevention, prompt diagnosis and therapy are critical to improve the prognosis in patients with PHT. The severity of PHT is reflected by the hepatic venous portal pressure gradient, also known as the portal pressure gradient (PPG). PHT can be assessed either by TE or by directly measuring the portal pressure. In patients with chronic liver disease who exhibit no symptoms, PHT can be diagnosed during routine checkups by using TE.35 A study involving patients with recurrent hepatitis C infections post-liver transplantation reported that liver stiffness measured by TE significantly reflected PHT with high sensitivity and specificity.36 In the latter approach, an interventional radiologist can measure portal pressure by assessing PPG via accessing the right jugular vein. EUS-enabled vascular intervention through PV catheterization was developed to address the limitation to assess PV pressure accurately. Initially tested in swine models, the method, which appeared feasible and safe, directly measured PPG with high accuracy and strongly correlated with the standard transjugular approach.37-43 It was then proven effective in humans,44 and a later prospective study of 28 patients showed high efficacy in assessing PPG without adverse effects.45,46 However, further studies are required to validate its application in clinical settings. Interestingly, a recent study showed the technical aspects, safety and feasibility of EUS-guided blood sampling from the portal circulation and its application in metabolomic profiling.47

4. Varices

During the last decade, the application of EUS to diagnose and manage gastric and esophageal varices has largely expanded. It can predict the risk of variceal bleeding and recurrent bleeding.48 Conventionally, esophagogastroduodenoscopy (EGD) was used to detect esophageal varices. Early reports showed EUS to be less effective than EGD, with several studies reporting that EUS was less accurate, and its sensitivity was largely dependent on the size and grade of varices.49,50 However, recent studies reported EUS to be comparable to EGD in detecting esophageal varices. In a study involving 66 patients diagnosed with cirrhosis, EUS could detect esophageal varices in 48 patients compared to 49 patients identified by EGD.51 Furthermore, EUS is reported to have a high sensitivity of 96.4% compared to standard EGD in cirrhotic patients.52 Moreover, improvising the EUS modality using smaller echo-endoscope tips and increased video resolution significantly increased the performance of EUS in diagnosing small esophageal varices.53-56 EUS-Doppler was shown to detect gastric and esophageal varices with high sensitivity, and it was also shown to be valuable in evaluating ectopic duodenal varices.57-64

In addition, EUS is also beneficial in predicting the risk of variceal recurrence after sclerotherapy or band ligation. A study of 38 patients who underwent sclerotherapy for esophageal varices and followed up for 2 years with EUS, reported that EUS could predict variceal recurrence risk as early as 3 to 4 months in advance.65 Another study evaluating EUS characteristics pre- and post-band ligation for first esophageal variceal bleeding showed the presence of para-esophageal veins larger than 4 mm post-band ligation to be an accurate predictive factor for variceal recurrence within a year, with a sensitivity and specificity of 70.6% and 84.6%, respectively.66 EUS may also be useful in predicting the risk of recurrent variceal bleeding, as shown in a retrospective study involving 306 patients who underwent endoscopic sclerotherapy for esophageal varices. The study reported that the increased occurrence of perforating veins before undergoing therapy and increased appearance of intramural cardiac veins, perforating veins, and the inflowing type of perforating veins 3 to 5 months post-therapy were associated with recurrent bleeding within a year of therapy.67

1. Liver diseases

LB remains the standard diagnostic tool for staging fibrosis in patients with chronic liver diseases, as well as identifying the etiology of liver disease.68 Conventionally, LB was performed via percutaneous, surgical, and transjugular approaches, but its application was limited due to its invasiveness and associated complications.69 Over the last two decades, and since it was first described in 2007,70 EUS-LB as evolved as an alternative technique for tissue sampling with proven safety and efficacy and with limited adverse events. Several studies have evaluated the efficacy, output, safety, and accuracy of EUS-LB for chronic liver disease.

Core biopsy needles have been exclusively used for EUS-LB rather than conventional fine needles. Using this approach, the liver lobes are identified by the echo-endoscope: left lobe from the stomach and right lobe from the duodenal bulb.71 Color Doppler imaging is used to carefully navigate the needle and care is taken to avoid vascular structures along the needle path.72 Both EUS-FNA and fine-needle biopsy (FNB) can be used in EUS-LB. EUS-guided LB with a 19-gauge FNA has been shown to be safe with comparable or higher yield than the percutaneous or transjugular approach.73

In a study by Stavropoulos et al.,74 EUS-LB using a 19-gauge fine needle was confirmed to be significantly successful with adequate tissue acquisition. Furthermore, the 19-gauge FNA compared to the 22-gauge FNB was confirmed to be superior with tissue adequacy in terms of sample length and reduced tissue fragmentation.75,76 A prospective study compared the 19-gauge FNA with 19-gauge FNB and reported FNB to have excellent performance for biopsy length and complete portal triads (CPT).77 However, a recent meta-analysis study reported FNA needles to be superior to FNB needles in tissue acquisition, with a 95.8% diagnostic yield and 0.9% rate of adverse events.78 In terms of tissue adequacy, 19-gauge FNA needle outperformed 22-gauge FNB needle as well as Tru-cut and non-Tru-cut 19-gauge FNB needles.79 Also, FNA was sufficient to harvest samples for cytological assessments, whereas FNB was the preferred method for harvesting samples for observing tissue architecture, molecular analysis, and immunohistochemistry.80 Moreover, EUS-LB enables sampling of both left and right liver lobes in a single session, which generally improves fibrosis assessment and management and reduces morbidity and mortality risks.5,81 Several tissue acquisition techniques have been proposed to improve the diagnostic yield of EUS-LB. The common ones include dry heparin, dry suction technique (DRST) and wet suction technique (WEST). A prospective study found WEST to be superior in tissue acquisition with greater cellularity and improved yield compared with DRST.82 The yield was further improvised using heparin needles to prevent coagulation. Another prospective study comparing DRST, dry heparin, and wet heparin techniques to harvest LB specimens showed wet heparin to be superior to the dry methods. Specimens harvested with wet heparin method had less tissue fragmentation, produced more CPT, and maintained increased aggregate specimen length and longer lengths of the longest piece.83 These techniques are useful with FNA needles and studies are limited for such applications using FNB needles. One method is the modified one-pass one actuation WEST. A retrospective study explained this technique with a 19-gauge EUS-FNB (SharkCore) needle in patients with abnormal liver chemistries with median total specimen length of 6 cm and mean CPT of 7.5, suggesting it to be an effective method.84

2. Nonalcoholic fatty liver disease

As the prevalence of obesity and metabolic syndrome is increasing globally, nonalcoholic fatty liver disease (NAFLD) has become the most common cause of liver disease and the leading indication for liver transplant in many countries.85 Accurate and timely diagnosis is critical for NAFLD management, and despite emerging non-invasive modalities, LB remains the gold standard,85,86 but EUS-LB is emerging as an alternative modality to diagnose fibrosis and the etiology of liver disease.87 In a large cohort study involving 47 patients with fatty liver who underwent EUS-FNB with 19-gauge SharkCore needle biopsy, the diagnostic yield and technical success were reported to be significantly higher, with only two patients developing minor adverse effects.88 Compared to magnetic resonance elastography, the 19-gauge core biopsy needle with the use of the modified one-pass wet suction method was more accurate in diagnosing and staging NAFLD.88 Another study reported a similar efficacy and safety rate using 22-gauge SharkCore needle biopsy among 21 NAFLD individuals, with minimal adverse events observed in six patients.87

There are several advantages to EUS-LB, including established safety and efficacy in delivering superior LB cores, easy access to bilobar biopsy, and cost and time efficiency when combined with other endoscopic procedures.89 Despite the advantages, EUS-LB has some limitations associated with its use. It is a relatively new technique and clinicians accustomed to traditional methods may find it challenging to use the EUS method as it requires a higher level of technical skills.78,90 Given the advantages and disadvantages, a multidisciplinary team approach may be beneficial in deciding between traditional and EUS methods to perform LB, reduce the challenges and improve cost and time efficiency.

1. Hepatic cysts

Simple hepatic cysts are mostly benign, asymptomatic and incidentally found in 2.5% to 7% of the population during routine screening.91 Of these benign cysts, 10% to 16% develop symptoms, such as abdominal pain and distension, among other complications that require further treatment. Conventionally, surgical therapy was considered the treatment option for symptomatic cysts, but the approach was associated with increased morbidity.92 While percutaneous aspiration was considered in certain circumstances, the method was associated with a recurrence rate of almost 100% within 2 years.93 Nevertheless, percutaneous aspiration followed by ethanol lavage was effective and safe in treating hepatic cysts with no recurrence observed in the 6 to 18 months follow-up period.94 In a retrospective study, Lee et al.95 studied the effectiveness of ethanol lavage therapy via percutaneous aspiration and EUS-guided approach in a total of 17 patients. Of the 19 hepatic cysts with a median cyst volume of 368.9 mL, 10 cysts were drained with the percutaneous approach and eight with the EUS-guided approach. Within the 15-month follow-up, the EUS-guided therapy approach was found to have a 100% reduction of cysts at a median 15-month follow-up, while the percutaneous approach had a 97.5% reduction at a median 11-month follow-up. Moreover, the EUS-guided drainage was exceptionally safe and feasible for cysts on the left hepatic lobe and the percutaneous approach for cysts on the right hepatic lobe.

2. Hepatic abscesses

Similar to hepatic cysts, hepatic abscesses are traditionally treated using surgical or percutaneous methods.96,97 Unfortunately, the percutaneous approach also has limitations due to possible organ injury and bleeding.98,99 EUS-guided hepatic abscess drainage is considered a safe and efficient alternative to traditional modalities to overcome these barriers. It can provide excellent visualization of the abscess, and the proximity can aid in direct needle access into the abscess cavity.100 In a case series presented with three hepatic abscesses localized to the caudate lobe and the gastro-hepatic space that were technically challenging to drain by percutaneous method, EUS-guided drainage could effectively drain the abscesses and showed complete resolution on follow-up.101 Later, several case studies reported successful drainage of hepatic abscesses using EUS-guided method via trans-gastric and trans-duodenal approaches.102-106 In a retrospective analysis involving 27 patients who underwent either EUS-guided drainage or percutaneous drainage, the EUS-guided group demonstrated a higher clinical success rate than the percutaneous group, at 100% and 82%, respectively.107 Further studies are required to validate its efficacy in standard practice. The procedure may be limited to abscesses localized in the left lobe; as for the right lobe, percutaneous drainage remains the traditional approach.

3. Variceal bleeding and PHT

In the last two decades, there has been a growing interest in using EUS not only for the early diagnosis of PHT but also for the treatment of varices. A pilot study on modified endoscopic variceal ligation technique using EUS-Doppler to reduce variceal recurrence was shown to be superior and successful in preventing variceal recurrence compared to endoscopic variceal ligation performed using traditional upper endoscopy. This was mainly because the EUS-guided approach aids in the exact localization and helps to completely eradicate the varices.108 Also, five patients in Spain were initially treated for gastric varices (GV) by EUS-guided injection of cyanoacrylate (CYA) in perforating feeding veins, which proved to be safe and efficient in achieving variceal obturation.109 Later, a multicenter, retrospective study showed that EUS-guided CYA injection was marginally better than EUS-guided coil application (ECA) in achieving GV obliteration (94.7% in patients treated with CYA injection versus 90.9% in patients treated with ECA).110 However, ECA had significantly fewer adverse events and required fewer endoscopies than CYA injection.109 Almost half the patients treated with CYA injection (47%) developed asymptomatic pulmonary embolism, while there were none in the group of patients treated with ECA. None of the patients showed recurrent GV during the 6 months follow-up period.109 In another recent randomized controlled study, both conventional endoscopic CYA injection and EUS-guided combined application of coil and CYA reported a similar efficacy in varices obliteration, and there were no significant differences in the two methods regarding embolism occurrence.111 However, patients treated with conventional CYA injection alone showed a greater tendency to develop embolism.111 A single-center randomized controlled study comparing EUS-guided coil and CYA injection versus EUS-guided coil injection alone for GV therapy reported superior clinical excellence, with low rates of rebleeding and reintervention in patients treated with coil and CYA combination compared to coil alone. Significant, immediate disappearance of varices was observed in patients treated with a combination of coil and CYA versus coil alone (86.7% vs 13.3%, p<0.001).112 Another study comparing EUS-guided fine-needle injection (EUS-FNI) of CYA versus direct endoscopic injection of CYA showed GV rebleeding rates of 8.8% and 23.7%,113 and similar adverse event rates of 20.3% and 17.5% in patients treated with EUS-FNI-CYA and direct endoscopic injection of CYA, respectively. Moreover, EUS-guided coil injection with absorbable gelatin sponge was reported to be superior to conventional CYA injection with fewer complications (10% vs 20%) and without rebleeding occurrence (0% vs 38%) at 9 months follow-up.114 Interestingly, a recent meta-analysis comparing the efficacy and safety of EUS-guided therapy (coil and/or CYA) versus conventional endoscopic CYA injection to treat GV reported that EUS-guided therapy had a better clinical efficacy in terms of recurrence and long-term rebleeding.115 GV obliteration was significantly better with EUS-guided therapy (84.4%; 95% confidence interval, 74.8% to 90.9%; I2=77) than the conventional CYA injection (62.6%; 95% confidence interval, 42.6% to 79.1%; I2=97, p=0.02).115 A study evaluating the long-term outcomes of EUS-guided injection of coil and CYA to treat gastric fundal varices reported superior efficacy for hemostasis in active bleeding and primary and secondary bleeding prophylaxis.116 Finally, a recent study with 80 patients confirmed the safety and efficacy of EUS-guided coil and glue injection for the primary prophylaxis of gastric variceal hemorrhage.117 In 2021, Thiruvengadam and Sedarat118 published a review summarizing some of these results.

In addition, esophageal varices can be eliminated entirely using EUS-guided sclerotherapy with less frequent recurrence.119,120

EUS-guided CYA injection with or without coiling is also beneficial in eradicating duodenal varices,60,61,121 with far less adverse effects compared to endoscopy-guided CYA injection.122

Although transjugular intrahepatic portosystemic shunt has been the standard therapy for PHT complications or refractory variceal bleeding, the EUS-guided intrahepatic portosystemic shunt was introduced as a safe alternative to overcome the challenges of the transjugular intrahepatic portosystemic shunt, as it does not include catheterization into the heart or inferior vena cava.123-125 Furthermore, it reduces radiation exposure risks to both patient and physician during stent placement.

Owing to its high performance, there is an increase in the use of artificial intelligence (AI) for medical image diagnosis. Deep learning, a type of AI algorithm, is an advanced machine learning technique based on neural networks being used for medical diagnosis.126,127 In the gastroenterological field, in relation to EUS images, AI is used to detect and distinguish anatomical features. A recent study by Marya et al.,128 developed a novel EUS-based convolutional neural network model to identify and classify focal liver lesions. The study demonstrated the model’s ability to autonomously identify focal liver lesions and accurately distinguish between benign and malignant lesions. Unique EUS images were used to train, validate, and test the model. For classifying malignant lesions, the model reported a sensitivity and specificity of 90% and 71%, respectively (AUROC, 0.861) while evaluating still images; while evaluating full-length videos, sensitivity and specificity of 100% and 80%, respectively (AUROC, 0.904) were observed. Using AI to evaluate EUS images for the diagnosis of liver diseases is relatively new and warrants more studies to validate its use in clinical settings.

Potential limitations of EUS include higher costs, risks associated with invasive procedures, and lack of EUS modalities in some hospitals. The major limitations of EUS are challenges in examining the right liver lobe. The accuracy of this modality is limited for lesions presented in the right liver lobe or under the dome of the diaphragm, and accurate diagnosis of other regions of the liver is unclear. Despite the effectiveness of EUS-guided LB, it is difficult to perform an accurate target biopsy in the right liver lobe. More evidence is required to establish its efficacy for lesions presented in the left liver lobe. In addition, the endosonographer’s expertise and skills to carefully scrutinize the liver are of critical diagnostic importance. Finally, most of the current studies analyzing EUS’s efficacy are single-center, non-randomized, and retrospective analysis; therefore, adequately designed, large, multicenter randomized controlled studies are required to widely establish its use in clinical settings.

In recent years, the role of EUS has significantly evolved with emerging applications in both diagnostic and therapeutic hepatology (Table 1). Owing to its excellent, unobstructed, real-time liver imaging, EUS is presented as a valuable tool for gastroenterologists and hepatologists to manage liver diseases and associated complications. EUS modalities leaped in several aspects, including improved visualization of focal liver lesions, tissue acquisition, and diagnosing gastric and esophageal varices. Moreover, EUS-guided interventional methods to assess portal pressure, drain hepatic abscesses, and ablate hepatic cysts are patient-friendly with limited risk of complications. In addition to diagnostic utilities, EUS is also considered a valuable and relatively safe and effective therapeutic modality for many applications in patients with chronic liver diseases. Given the several advantages and strengths of EUS, its clinical applications are expected to rapidly grow in all aspects of diagnostic and therapeutic hepatology.

Table 1. Advantages of EUS and EUS-Guided Techniques

Diagnostic applications of EUS
Focal liver lesions
  • Can simultaneously evaluate the appearance of focal liver lesions and harvest samples of lesions for histological analysis

  • Outperforms in its diagnostic accuracy by diagnosing lesions smaller than 10 mm

  • Can detect a higher number of hepatic metastatic lesions compared to CT

  • EUS-elastography: efficient in identifying, differentiating, and characterizing between malignant and benign hepatic focal lesions

  • CE-EUS: superior accuracy in detecting deep liver lesions over CE-US

Liver cirrhosis
  • EUS-guided liver stiffness measurements can accurately assess liver fibrosis in obese patients and in individuals with ascites

  • EUS RTE: high sensitivity than transabdominal RTE in evaluating liver fibrosis

  • EUS: superior in detecting gastroesophageal varices in early cirrhosis

Portal hypertension
  • EUS-enabled vascular intervention through PV catheterization can accurately assess PV pressure

Varices
  • High sensitivity compared to standard EGD in cirrhotic patients

  • EUS-Doppler can detect gastric and esophageal varices with high sensitivity

  • Valuable in evaluating ectopic duodenal varices

  • Beneficial in predicting the risk of variceal recurrence after sclerotherapy or band ligation

  • Useful in predicting the risk of recurrent variceal bleeding

EUS-guided liver biopsy
  • Proven safety and efficacy with limited adverse events

  • Yields superior liver biopsy cores

  • Easy access to bilobar biopsy

  • Cost and time efficiency when combined with other endoscopic procedures

Therapeutic applications of EUS
Hepatic cysts
  • Results in complete reduction of cysts

  • Exceptionally safe and feasible for cysts on the left hepatic lobe

Hepatic abscesses
  • EUS-guided hepatic abscess drainage: Safe and efficient alternative to traditional modalities to overcome possible organ injury and bleeding

  • Provides excellent visualization of the abscess

  • Proximity can aid in the direct needle access into the abscess cavity

  • Results in complete resolution

  • Higher clinical success rate than the percutaneous method

Variceal bleeding and portal hypertension
  • Successful in preventing variceal recurrence compared to EVL performed using traditional upper endoscopy

  • Aids in the exact localization and helps to completely eradicate the varices

  • Superior clinical excellence, with low rates of rebleeding and reintervention in patients treated with EUS-guided coil and CYA combination

  • EUS-guided coil injection with absorbable gelatin sponge was superior to conventional CYA injection with fewer complications

  • GV obliteration was significantly better with EUS-guided therapy

  • EUS-guided intrahepatic portosystemic shunt is a safe alternative to TIPS, as it does not include catheterization into the heart or IVC

EUS, endoscopic ultrasound; CT, computer tomography; CE, contrast enhancement; US, ultrasound; RTE, real-time elastography; PV, portal vein; EGD, esophagogastroduodenoscopy; EVL, endoscopic variceal ligation; CYA, cyanoacrylate; GV, gastric varices; TIPS, transjugular intrahepatic portosystemic shunt; IVC, inferior vena cava.


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Gut and Liver

Published online December 2, 2022

Copyright © Gut and Liver.

The Role of Endoscopic Ultrasound in Hepatology

Saleh A. Alqahtani1,2 , Floriane Ausloos3 , Ji Seok Park4 , Sunguk Jang4

1Division of Gastroenterology and Hepatology, Johns Hopkins University, Baltimore, MD, USA, 2Liver Transplant Centre, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia, 3Department of Gastroenterology and Hepatology, CHU Liège, Sart-Tilman, Liège, Belgium, and 4Department of Gastroenterology and Hepatology, Digestive Disease Institute, Cleveland Clinic, Cleveland, OH, USA

Correspondence to:Sunguk Jang
ORCID https://orcid.org/0000-0001-9837-0322
E-mail jangs@ccf.org

Received: February 22, 2022; Revised: May 19, 2022; Accepted: June 21, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Endoscopic ultrasound (EUS) has been an indispensable and widely used diagnostic tool in several medical fields, including gastroenterology, cardiology, and urology, due to its diverse therapeutic and diagnostic applications. Many studies show that it is effective and safe in patients with liver conditions where conventional endoscopy or cross-sectional imaging are inefficient or when surgical interventions pose high risks. In this article, we present a review of the current literature for the different diagnostic and therapeutic applications of EUS in liver diseases and their complications and discuss the potential future application of artificial intelligence analysis of EUS.

Keywords: Endoscopic ultrasound, Liver diseases, Portal hypertension

INTRODUCTION

Endoscopic ultrasound (EUS) has been an indispensable and widely used diagnostic tool since its initial description in the 1980s. Its diverse therapeutic and diagnostic applications have allowed for its use in various medical field, including gastroenterology, cardiology, and urology.1,2 In recent years, EUS has also proven effective and safe in patients with liver conditions where conventional endoscopy or cross-sectional imaging are inefficient and when surgical interventions pose high risks. Growing evidence shows that expanding therapeutic and diagnostic applications of EUS, especially in managing chronic hepatic diseases, outperform in accuracy compared to conventional imaging techniques, such as transabdominal ultrasound (US) and computer tomography (CT). More specifically, a major advantage of EUS is the proximity and ease of using the EUS transducer close to the liver and accurately identifying blood vessels and other intervening structures.3 Due to its superior performance and negligible adverse effects, EUS has been a highly preferred tool in identifying, characterizing, and staging primary and malignant liver tumors.4-6

Moreover, newly emerging echoendoscopes are provided with color, power and pulsed Doppler, enabling them to identify blood vessels and measure portal pressure in blood vessels.7,8 Combined EUS with real-time elastography (RTE) can effectively measure stiffness of the liver parenchyma and focal lesions.7 In addition, liver biopsy (LB) guided by EUS is safer with lower risks than the traditional percutaneous method.9

In this review, we discuss in detail previous and recent applications of EUS as a diagnostic and therapeutic tool in managing liver diseases and explain the potential future use of artificial intelligence analysis for EUS.

DIAGNOSTIC APPLICATIONS OF EUS

1. Focal liver lesions

EUS has the advantage of evaluating the appearance of focal liver lesions and taking samples of lesions for histological diagnosis. Focal liver lesions include benign (hepatic abscess, hepatic cyst, hemangioma, and hepatocellular adenoma) and malignant lesions (hepatocellular carcinoma [HCC], cholangiocarcinoma, and liver metastasis) and are traditionally diagnosed using conventional methods, such as transabdominal imaging and percutaneous tissue sampling. In most cases, focal liver lesions are incidentally found using cross-sectional imaging with US, CT, or magnetic resonance imaging in patients at high risk for hepatic malignancies.6,10 Understanding the nature of these lesions is extremely important for the prognosis of hepatic malignancies. However, conventional screening using US, CT, and magnetic resonance imaging has its limitations in accurately diagnosing the nature of these lesions, especially for smaller lesions (<10 mm).11,12 EUS outperforms in its diagnostic accuracy compared to these traditional modalities with the power to diagnose lesions smaller than 10 mm.6,13 In a prospective study in patients with gastrointestinal or pulmonary malignancies, EUS identified liver lesions with high accuracy in 14 patients compared to CT, which only detected three of the lesions.14 More studies have validated the superiority of EUS over CT by accurately detecting lesions <5 mm in diameter.15,16 In fact, one of these studies showed that EUS detected an additional 28% of hepatic lesions among 14 patients with a history of suspected hepatic malignancies previously detected by CT.15 Diagnostic accuracy of EUS and CT for detecting hepatic lesions were found to be 98% and 92%, respectively, with EUS significantly detecting a higher number of hepatic metastatic lesions compared to CT.16

Elastography is a noninvasive method using US waves to assess liver stiffness. It has a strong correlation with the degree of liver fibrosis demonstrated by LB. However, the technique is limited to people with ascites, narrow intercostal spaces, and body habitus.17 EUS elastography can overcome most of these limitations and has been described as a significant tool in identifying, differentiating, and characterizing malignant and benign hepatic focal lesions with a diagnostic accuracy, sensitivity, and specificity of 88.6%, 92.5%, and 88.8%, respectively.18-20 Malignant liver masses are stiffer than benign masses, and EUS elastography's ability to quantify the stiffness has rendered it a valuable tool in characterizing liver lesions.21

In addition, hepatic microvascular architecture can be better visualized using contrast agents. Contrast enhancement (CE) is widely used to improve the diagnostic performance of US and EUS. Contrast-enhanced-EUS (CE-EUS) is classified into CE-EUS with the Doppler method and CE-EUS with harmonic imaging, which allows improved detection and characterization of focal liver lesions.22 Like CE-US, CE-EUS can be used to detail different types of liver lesions through vascular enhancement patterns, with typical patterns including arterial hyperenhancement: (1) subsequent wash out in late-phase contrast in HCC; (2) rim-like enhancement and subsequent rapid washout in metastatic hepatic cancer; (3) with progressive, early, spoke-wheel arteries, unenhanced central scar in focal nodular hyperplasia, and peripheral nodular hyperenhancement; (4) with centripetal progressive fill-in hemangioma.23-25

Moreover, CE-US has been demonstrated to be a valuable tool to evaluate the effectiveness of HCC treatment with a sensitivity and accuracy of 95.6% and 96.2%, respectively, and to detect residual tumor with a sensitivity and accuracy of 76.2% and 77.7%, respectively.26 Given these observations, CE-EUS could be of potential value with superior accuracy in detecting deep liver lesions over CE-US.27 However, further studies are required to validate it.

In a retrospective analysis, Fujii-Lau et al.28 developed a EUS scoring system to distinguish between benign and malignant hepatic masses by analyzing data from patients who underwent EUS-fine needle aspiration (FNA) of solid hepatic masses. The derived and validated EUS criteria showed a high positive predictive value of 88% and could detect radiographically occult masses <5 mm. Moreover, the scoring system could enable endosonographers to make informed decisions to avoid unnecessary FNA interventions. Multicenter studies involving multiple endosonographers are required to further validate the scoring system. The algorithm is described in Fig. 1.

Figure 1. Scoring system based on sonographic criteria in distinguishing benign lesion from malignant lesion.

2. Liver cirrhosis

LB is the gold standard diagnostic tool for liver cirrhosis; however, its application is limited due to sampling errors, complications associated with it being an invasive procedure, inter-observer variability, and cost.29 Several noninvasive modalities, based on noninvasive fibrosis markers, such as transient elastography (TE), and RTE to measure liver stiffness, have been developed to overcome these limitations.30 Nonetheless, the performance to detect fibrosis is suboptimal as the transabdominal approach is limited in obese patients and individuals with ascites.29 In such scenarios, EUS-guided liver stiffness measurements are advantageous and can overcome barriers given the transducer's proximity to the liver, thereby accurately assessing liver fibrosis.31 Moreover, EUS RTE is more sensitive than transabdominal RTE in evaluating liver fibrosis because the signal passes through the thin gastric wall versus the abdominal wall in transabdominal RTE.32 Liver fibrosis index, calculated using EUS RTE images, significantly correlates with transabdominal imaging and can accurately stratify normal, fatty, and cirrhotic livers.32 Given these advantages, EUS RTE can be both an effective and time-efficient modality for assessing fibrosis in patients with liver diseases, especially when patients undergo upper endoscopy for variceal screening or other indications. Furthermore, additional information about liver parenchyma can be obtained all in one session.

Another study evaluating the diagnostic value of EUS, Fibroscan, and acoustic radiation force impulse to detect esophagogastric varices, liver stiffness measurement, and liver virtual touch tissue quantification, respectively, in patients with chronic viral liver disease, reported significantly higher detection rate for early-stage liver cirrhosis (Child-Pugh A grade) than chronic hepatitis. Moreover, the combination of these three modalities had a superior diagnostic value for early-stage liver cirrhosis.33 The regression model of EUS, Fibroscan, and acoustic radiation force impulse reported an area under the receiver operating characteristic curve (AUROC) of 0.947 with a sensitivity and specificity of 0.878 and 0.867, respectively.

These results suggest a promising role for EUS along with other modalities in early and accurate diagnosis of complications in early liver cirrhosis and may improve the diagnosis rate and decrease the misdiagnosis rate.

3. Portal hypertension

Cirrhosis can lead to portal hypertension (PHT), defined as a major hemodynamic shift due to increased pressure in the portal vein (PV), and correlates to complications, such as ascites, variceal bleeding, and encephalopathy.34 Thus, prevention, prompt diagnosis and therapy are critical to improve the prognosis in patients with PHT. The severity of PHT is reflected by the hepatic venous portal pressure gradient, also known as the portal pressure gradient (PPG). PHT can be assessed either by TE or by directly measuring the portal pressure. In patients with chronic liver disease who exhibit no symptoms, PHT can be diagnosed during routine checkups by using TE.35 A study involving patients with recurrent hepatitis C infections post-liver transplantation reported that liver stiffness measured by TE significantly reflected PHT with high sensitivity and specificity.36 In the latter approach, an interventional radiologist can measure portal pressure by assessing PPG via accessing the right jugular vein. EUS-enabled vascular intervention through PV catheterization was developed to address the limitation to assess PV pressure accurately. Initially tested in swine models, the method, which appeared feasible and safe, directly measured PPG with high accuracy and strongly correlated with the standard transjugular approach.37-43 It was then proven effective in humans,44 and a later prospective study of 28 patients showed high efficacy in assessing PPG without adverse effects.45,46 However, further studies are required to validate its application in clinical settings. Interestingly, a recent study showed the technical aspects, safety and feasibility of EUS-guided blood sampling from the portal circulation and its application in metabolomic profiling.47

4. Varices

During the last decade, the application of EUS to diagnose and manage gastric and esophageal varices has largely expanded. It can predict the risk of variceal bleeding and recurrent bleeding.48 Conventionally, esophagogastroduodenoscopy (EGD) was used to detect esophageal varices. Early reports showed EUS to be less effective than EGD, with several studies reporting that EUS was less accurate, and its sensitivity was largely dependent on the size and grade of varices.49,50 However, recent studies reported EUS to be comparable to EGD in detecting esophageal varices. In a study involving 66 patients diagnosed with cirrhosis, EUS could detect esophageal varices in 48 patients compared to 49 patients identified by EGD.51 Furthermore, EUS is reported to have a high sensitivity of 96.4% compared to standard EGD in cirrhotic patients.52 Moreover, improvising the EUS modality using smaller echo-endoscope tips and increased video resolution significantly increased the performance of EUS in diagnosing small esophageal varices.53-56 EUS-Doppler was shown to detect gastric and esophageal varices with high sensitivity, and it was also shown to be valuable in evaluating ectopic duodenal varices.57-64

In addition, EUS is also beneficial in predicting the risk of variceal recurrence after sclerotherapy or band ligation. A study of 38 patients who underwent sclerotherapy for esophageal varices and followed up for 2 years with EUS, reported that EUS could predict variceal recurrence risk as early as 3 to 4 months in advance.65 Another study evaluating EUS characteristics pre- and post-band ligation for first esophageal variceal bleeding showed the presence of para-esophageal veins larger than 4 mm post-band ligation to be an accurate predictive factor for variceal recurrence within a year, with a sensitivity and specificity of 70.6% and 84.6%, respectively.66 EUS may also be useful in predicting the risk of recurrent variceal bleeding, as shown in a retrospective study involving 306 patients who underwent endoscopic sclerotherapy for esophageal varices. The study reported that the increased occurrence of perforating veins before undergoing therapy and increased appearance of intramural cardiac veins, perforating veins, and the inflowing type of perforating veins 3 to 5 months post-therapy were associated with recurrent bleeding within a year of therapy.67

EUS-GUIDED LB

1. Liver diseases

LB remains the standard diagnostic tool for staging fibrosis in patients with chronic liver diseases, as well as identifying the etiology of liver disease.68 Conventionally, LB was performed via percutaneous, surgical, and transjugular approaches, but its application was limited due to its invasiveness and associated complications.69 Over the last two decades, and since it was first described in 2007,70 EUS-LB as evolved as an alternative technique for tissue sampling with proven safety and efficacy and with limited adverse events. Several studies have evaluated the efficacy, output, safety, and accuracy of EUS-LB for chronic liver disease.

Core biopsy needles have been exclusively used for EUS-LB rather than conventional fine needles. Using this approach, the liver lobes are identified by the echo-endoscope: left lobe from the stomach and right lobe from the duodenal bulb.71 Color Doppler imaging is used to carefully navigate the needle and care is taken to avoid vascular structures along the needle path.72 Both EUS-FNA and fine-needle biopsy (FNB) can be used in EUS-LB. EUS-guided LB with a 19-gauge FNA has been shown to be safe with comparable or higher yield than the percutaneous or transjugular approach.73

In a study by Stavropoulos et al.,74 EUS-LB using a 19-gauge fine needle was confirmed to be significantly successful with adequate tissue acquisition. Furthermore, the 19-gauge FNA compared to the 22-gauge FNB was confirmed to be superior with tissue adequacy in terms of sample length and reduced tissue fragmentation.75,76 A prospective study compared the 19-gauge FNA with 19-gauge FNB and reported FNB to have excellent performance for biopsy length and complete portal triads (CPT).77 However, a recent meta-analysis study reported FNA needles to be superior to FNB needles in tissue acquisition, with a 95.8% diagnostic yield and 0.9% rate of adverse events.78 In terms of tissue adequacy, 19-gauge FNA needle outperformed 22-gauge FNB needle as well as Tru-cut and non-Tru-cut 19-gauge FNB needles.79 Also, FNA was sufficient to harvest samples for cytological assessments, whereas FNB was the preferred method for harvesting samples for observing tissue architecture, molecular analysis, and immunohistochemistry.80 Moreover, EUS-LB enables sampling of both left and right liver lobes in a single session, which generally improves fibrosis assessment and management and reduces morbidity and mortality risks.5,81 Several tissue acquisition techniques have been proposed to improve the diagnostic yield of EUS-LB. The common ones include dry heparin, dry suction technique (DRST) and wet suction technique (WEST). A prospective study found WEST to be superior in tissue acquisition with greater cellularity and improved yield compared with DRST.82 The yield was further improvised using heparin needles to prevent coagulation. Another prospective study comparing DRST, dry heparin, and wet heparin techniques to harvest LB specimens showed wet heparin to be superior to the dry methods. Specimens harvested with wet heparin method had less tissue fragmentation, produced more CPT, and maintained increased aggregate specimen length and longer lengths of the longest piece.83 These techniques are useful with FNA needles and studies are limited for such applications using FNB needles. One method is the modified one-pass one actuation WEST. A retrospective study explained this technique with a 19-gauge EUS-FNB (SharkCore) needle in patients with abnormal liver chemistries with median total specimen length of 6 cm and mean CPT of 7.5, suggesting it to be an effective method.84

2. Nonalcoholic fatty liver disease

As the prevalence of obesity and metabolic syndrome is increasing globally, nonalcoholic fatty liver disease (NAFLD) has become the most common cause of liver disease and the leading indication for liver transplant in many countries.85 Accurate and timely diagnosis is critical for NAFLD management, and despite emerging non-invasive modalities, LB remains the gold standard,85,86 but EUS-LB is emerging as an alternative modality to diagnose fibrosis and the etiology of liver disease.87 In a large cohort study involving 47 patients with fatty liver who underwent EUS-FNB with 19-gauge SharkCore needle biopsy, the diagnostic yield and technical success were reported to be significantly higher, with only two patients developing minor adverse effects.88 Compared to magnetic resonance elastography, the 19-gauge core biopsy needle with the use of the modified one-pass wet suction method was more accurate in diagnosing and staging NAFLD.88 Another study reported a similar efficacy and safety rate using 22-gauge SharkCore needle biopsy among 21 NAFLD individuals, with minimal adverse events observed in six patients.87

There are several advantages to EUS-LB, including established safety and efficacy in delivering superior LB cores, easy access to bilobar biopsy, and cost and time efficiency when combined with other endoscopic procedures.89 Despite the advantages, EUS-LB has some limitations associated with its use. It is a relatively new technique and clinicians accustomed to traditional methods may find it challenging to use the EUS method as it requires a higher level of technical skills.78,90 Given the advantages and disadvantages, a multidisciplinary team approach may be beneficial in deciding between traditional and EUS methods to perform LB, reduce the challenges and improve cost and time efficiency.

THERAPEUTIC APPLICATIONS OF EUS

1. Hepatic cysts

Simple hepatic cysts are mostly benign, asymptomatic and incidentally found in 2.5% to 7% of the population during routine screening.91 Of these benign cysts, 10% to 16% develop symptoms, such as abdominal pain and distension, among other complications that require further treatment. Conventionally, surgical therapy was considered the treatment option for symptomatic cysts, but the approach was associated with increased morbidity.92 While percutaneous aspiration was considered in certain circumstances, the method was associated with a recurrence rate of almost 100% within 2 years.93 Nevertheless, percutaneous aspiration followed by ethanol lavage was effective and safe in treating hepatic cysts with no recurrence observed in the 6 to 18 months follow-up period.94 In a retrospective study, Lee et al.95 studied the effectiveness of ethanol lavage therapy via percutaneous aspiration and EUS-guided approach in a total of 17 patients. Of the 19 hepatic cysts with a median cyst volume of 368.9 mL, 10 cysts were drained with the percutaneous approach and eight with the EUS-guided approach. Within the 15-month follow-up, the EUS-guided therapy approach was found to have a 100% reduction of cysts at a median 15-month follow-up, while the percutaneous approach had a 97.5% reduction at a median 11-month follow-up. Moreover, the EUS-guided drainage was exceptionally safe and feasible for cysts on the left hepatic lobe and the percutaneous approach for cysts on the right hepatic lobe.

2. Hepatic abscesses

Similar to hepatic cysts, hepatic abscesses are traditionally treated using surgical or percutaneous methods.96,97 Unfortunately, the percutaneous approach also has limitations due to possible organ injury and bleeding.98,99 EUS-guided hepatic abscess drainage is considered a safe and efficient alternative to traditional modalities to overcome these barriers. It can provide excellent visualization of the abscess, and the proximity can aid in direct needle access into the abscess cavity.100 In a case series presented with three hepatic abscesses localized to the caudate lobe and the gastro-hepatic space that were technically challenging to drain by percutaneous method, EUS-guided drainage could effectively drain the abscesses and showed complete resolution on follow-up.101 Later, several case studies reported successful drainage of hepatic abscesses using EUS-guided method via trans-gastric and trans-duodenal approaches.102-106 In a retrospective analysis involving 27 patients who underwent either EUS-guided drainage or percutaneous drainage, the EUS-guided group demonstrated a higher clinical success rate than the percutaneous group, at 100% and 82%, respectively.107 Further studies are required to validate its efficacy in standard practice. The procedure may be limited to abscesses localized in the left lobe; as for the right lobe, percutaneous drainage remains the traditional approach.

3. Variceal bleeding and PHT

In the last two decades, there has been a growing interest in using EUS not only for the early diagnosis of PHT but also for the treatment of varices. A pilot study on modified endoscopic variceal ligation technique using EUS-Doppler to reduce variceal recurrence was shown to be superior and successful in preventing variceal recurrence compared to endoscopic variceal ligation performed using traditional upper endoscopy. This was mainly because the EUS-guided approach aids in the exact localization and helps to completely eradicate the varices.108 Also, five patients in Spain were initially treated for gastric varices (GV) by EUS-guided injection of cyanoacrylate (CYA) in perforating feeding veins, which proved to be safe and efficient in achieving variceal obturation.109 Later, a multicenter, retrospective study showed that EUS-guided CYA injection was marginally better than EUS-guided coil application (ECA) in achieving GV obliteration (94.7% in patients treated with CYA injection versus 90.9% in patients treated with ECA).110 However, ECA had significantly fewer adverse events and required fewer endoscopies than CYA injection.109 Almost half the patients treated with CYA injection (47%) developed asymptomatic pulmonary embolism, while there were none in the group of patients treated with ECA. None of the patients showed recurrent GV during the 6 months follow-up period.109 In another recent randomized controlled study, both conventional endoscopic CYA injection and EUS-guided combined application of coil and CYA reported a similar efficacy in varices obliteration, and there were no significant differences in the two methods regarding embolism occurrence.111 However, patients treated with conventional CYA injection alone showed a greater tendency to develop embolism.111 A single-center randomized controlled study comparing EUS-guided coil and CYA injection versus EUS-guided coil injection alone for GV therapy reported superior clinical excellence, with low rates of rebleeding and reintervention in patients treated with coil and CYA combination compared to coil alone. Significant, immediate disappearance of varices was observed in patients treated with a combination of coil and CYA versus coil alone (86.7% vs 13.3%, p<0.001).112 Another study comparing EUS-guided fine-needle injection (EUS-FNI) of CYA versus direct endoscopic injection of CYA showed GV rebleeding rates of 8.8% and 23.7%,113 and similar adverse event rates of 20.3% and 17.5% in patients treated with EUS-FNI-CYA and direct endoscopic injection of CYA, respectively. Moreover, EUS-guided coil injection with absorbable gelatin sponge was reported to be superior to conventional CYA injection with fewer complications (10% vs 20%) and without rebleeding occurrence (0% vs 38%) at 9 months follow-up.114 Interestingly, a recent meta-analysis comparing the efficacy and safety of EUS-guided therapy (coil and/or CYA) versus conventional endoscopic CYA injection to treat GV reported that EUS-guided therapy had a better clinical efficacy in terms of recurrence and long-term rebleeding.115 GV obliteration was significantly better with EUS-guided therapy (84.4%; 95% confidence interval, 74.8% to 90.9%; I2=77) than the conventional CYA injection (62.6%; 95% confidence interval, 42.6% to 79.1%; I2=97, p=0.02).115 A study evaluating the long-term outcomes of EUS-guided injection of coil and CYA to treat gastric fundal varices reported superior efficacy for hemostasis in active bleeding and primary and secondary bleeding prophylaxis.116 Finally, a recent study with 80 patients confirmed the safety and efficacy of EUS-guided coil and glue injection for the primary prophylaxis of gastric variceal hemorrhage.117 In 2021, Thiruvengadam and Sedarat118 published a review summarizing some of these results.

In addition, esophageal varices can be eliminated entirely using EUS-guided sclerotherapy with less frequent recurrence.119,120

EUS-guided CYA injection with or without coiling is also beneficial in eradicating duodenal varices,60,61,121 with far less adverse effects compared to endoscopy-guided CYA injection.122

Although transjugular intrahepatic portosystemic shunt has been the standard therapy for PHT complications or refractory variceal bleeding, the EUS-guided intrahepatic portosystemic shunt was introduced as a safe alternative to overcome the challenges of the transjugular intrahepatic portosystemic shunt, as it does not include catheterization into the heart or inferior vena cava.123-125 Furthermore, it reduces radiation exposure risks to both patient and physician during stent placement.

ARTIFICIAL INTELLIGENCE ANALYSIS FOR EUS AND THE FUTURE

Owing to its high performance, there is an increase in the use of artificial intelligence (AI) for medical image diagnosis. Deep learning, a type of AI algorithm, is an advanced machine learning technique based on neural networks being used for medical diagnosis.126,127 In the gastroenterological field, in relation to EUS images, AI is used to detect and distinguish anatomical features. A recent study by Marya et al.,128 developed a novel EUS-based convolutional neural network model to identify and classify focal liver lesions. The study demonstrated the model’s ability to autonomously identify focal liver lesions and accurately distinguish between benign and malignant lesions. Unique EUS images were used to train, validate, and test the model. For classifying malignant lesions, the model reported a sensitivity and specificity of 90% and 71%, respectively (AUROC, 0.861) while evaluating still images; while evaluating full-length videos, sensitivity and specificity of 100% and 80%, respectively (AUROC, 0.904) were observed. Using AI to evaluate EUS images for the diagnosis of liver diseases is relatively new and warrants more studies to validate its use in clinical settings.

LIMITATIONS OF EUS

Potential limitations of EUS include higher costs, risks associated with invasive procedures, and lack of EUS modalities in some hospitals. The major limitations of EUS are challenges in examining the right liver lobe. The accuracy of this modality is limited for lesions presented in the right liver lobe or under the dome of the diaphragm, and accurate diagnosis of other regions of the liver is unclear. Despite the effectiveness of EUS-guided LB, it is difficult to perform an accurate target biopsy in the right liver lobe. More evidence is required to establish its efficacy for lesions presented in the left liver lobe. In addition, the endosonographer’s expertise and skills to carefully scrutinize the liver are of critical diagnostic importance. Finally, most of the current studies analyzing EUS’s efficacy are single-center, non-randomized, and retrospective analysis; therefore, adequately designed, large, multicenter randomized controlled studies are required to widely establish its use in clinical settings.

CONCLUSION

In recent years, the role of EUS has significantly evolved with emerging applications in both diagnostic and therapeutic hepatology (Table 1). Owing to its excellent, unobstructed, real-time liver imaging, EUS is presented as a valuable tool for gastroenterologists and hepatologists to manage liver diseases and associated complications. EUS modalities leaped in several aspects, including improved visualization of focal liver lesions, tissue acquisition, and diagnosing gastric and esophageal varices. Moreover, EUS-guided interventional methods to assess portal pressure, drain hepatic abscesses, and ablate hepatic cysts are patient-friendly with limited risk of complications. In addition to diagnostic utilities, EUS is also considered a valuable and relatively safe and effective therapeutic modality for many applications in patients with chronic liver diseases. Given the several advantages and strengths of EUS, its clinical applications are expected to rapidly grow in all aspects of diagnostic and therapeutic hepatology.

Table 1 . Advantages of EUS and EUS-Guided Techniques.

Diagnostic applications of EUS
Focal liver lesions
  • Can simultaneously evaluate the appearance of focal liver lesions and harvest samples of lesions for histological analysis.

  • Outperforms in its diagnostic accuracy by diagnosing lesions smaller than 10 mm.

  • Can detect a higher number of hepatic metastatic lesions compared to CT.

  • EUS-elastography: efficient in identifying, differentiating, and characterizing between malignant and benign hepatic focal lesions.

  • CE-EUS: superior accuracy in detecting deep liver lesions over CE-US.

Liver cirrhosis
  • EUS-guided liver stiffness measurements can accurately assess liver fibrosis in obese patients and in individuals with ascites.

  • EUS RTE: high sensitivity than transabdominal RTE in evaluating liver fibrosis.

  • EUS: superior in detecting gastroesophageal varices in early cirrhosis.

Portal hypertension
  • EUS-enabled vascular intervention through PV catheterization can accurately assess PV pressure.

Varices
  • High sensitivity compared to standard EGD in cirrhotic patients.

  • EUS-Doppler can detect gastric and esophageal varices with high sensitivity.

  • Valuable in evaluating ectopic duodenal varices.

  • Beneficial in predicting the risk of variceal recurrence after sclerotherapy or band ligation.

  • Useful in predicting the risk of recurrent variceal bleeding.

EUS-guided liver biopsy
  • Proven safety and efficacy with limited adverse events.

  • Yields superior liver biopsy cores.

  • Easy access to bilobar biopsy.

  • Cost and time efficiency when combined with other endoscopic procedures.

Therapeutic applications of EUS
Hepatic cysts
  • Results in complete reduction of cysts.

  • Exceptionally safe and feasible for cysts on the left hepatic lobe.

Hepatic abscesses
  • EUS-guided hepatic abscess drainage: Safe and efficient alternative to traditional modalities to overcome possible organ injury and bleeding.

  • Provides excellent visualization of the abscess.

  • Proximity can aid in the direct needle access into the abscess cavity.

  • Results in complete resolution.

  • Higher clinical success rate than the percutaneous method.

Variceal bleeding and portal hypertension
  • Successful in preventing variceal recurrence compared to EVL performed using traditional upper endoscopy.

  • Aids in the exact localization and helps to completely eradicate the varices.

  • Superior clinical excellence, with low rates of rebleeding and reintervention in patients treated with EUS-guided coil and CYA combination.

  • EUS-guided coil injection with absorbable gelatin sponge was superior to conventional CYA injection with fewer complications.

  • GV obliteration was significantly better with EUS-guided therapy.

  • EUS-guided intrahepatic portosystemic shunt is a safe alternative to TIPS, as it does not include catheterization into the heart or IVC.

EUS, endoscopic ultrasound; CT, computer tomography; CE, contrast enhancement; US, ultrasound; RTE, real-time elastography; PV, portal vein; EGD, esophagogastroduodenoscopy; EVL, endoscopic variceal ligation; CYA, cyanoacrylate; GV, gastric varices; TIPS, transjugular intrahepatic portosystemic shunt; IVC, inferior vena cava..


CONFLICTS OF INTEREST

No potential conflict of interest relevant to this article was reported.

Fig 1.

Figure 1.Scoring system based on sonographic criteria in distinguishing benign lesion from malignant lesion.
Gut and Liver 2022; :

Table 1 Advantages of EUS and EUS-Guided Techniques

Diagnostic applications of EUS
Focal liver lesions

Can simultaneously evaluate the appearance of focal liver lesions and harvest samples of lesions for histological analysis

Outperforms in its diagnostic accuracy by diagnosing lesions smaller than 10 mm

Can detect a higher number of hepatic metastatic lesions compared to CT

EUS-elastography: efficient in identifying, differentiating, and characterizing between malignant and benign hepatic focal lesions

CE-EUS: superior accuracy in detecting deep liver lesions over CE-US

Liver cirrhosis

EUS-guided liver stiffness measurements can accurately assess liver fibrosis in obese patients and in individuals with ascites

EUS RTE: high sensitivity than transabdominal RTE in evaluating liver fibrosis

EUS: superior in detecting gastroesophageal varices in early cirrhosis

Portal hypertension

EUS-enabled vascular intervention through PV catheterization can accurately assess PV pressure

Varices

High sensitivity compared to standard EGD in cirrhotic patients

EUS-Doppler can detect gastric and esophageal varices with high sensitivity

Valuable in evaluating ectopic duodenal varices

Beneficial in predicting the risk of variceal recurrence after sclerotherapy or band ligation

Useful in predicting the risk of recurrent variceal bleeding

EUS-guided liver biopsy

Proven safety and efficacy with limited adverse events

Yields superior liver biopsy cores

Easy access to bilobar biopsy

Cost and time efficiency when combined with other endoscopic procedures

Therapeutic applications of EUS
Hepatic cysts

Results in complete reduction of cysts

Exceptionally safe and feasible for cysts on the left hepatic lobe

Hepatic abscesses

EUS-guided hepatic abscess drainage: Safe and efficient alternative to traditional modalities to overcome possible organ injury and bleeding

Provides excellent visualization of the abscess

Proximity can aid in the direct needle access into the abscess cavity

Results in complete resolution

Higher clinical success rate than the percutaneous method

Variceal bleeding and portal hypertension

Successful in preventing variceal recurrence compared to EVL performed using traditional upper endoscopy

Aids in the exact localization and helps to completely eradicate the varices

Superior clinical excellence, with low rates of rebleeding and reintervention in patients treated with EUS-guided coil and CYA combination

EUS-guided coil injection with absorbable gelatin sponge was superior to conventional CYA injection with fewer complications

GV obliteration was significantly better with EUS-guided therapy

EUS-guided intrahepatic portosystemic shunt is a safe alternative to TIPS, as it does not include catheterization into the heart or IVC

EUS, endoscopic ultrasound; CT, computer tomography; CE, contrast enhancement; US, ultrasound; RTE, real-time elastography; PV, portal vein; EGD, esophagogastroduodenoscopy; EVL, endoscopic variceal ligation; CYA, cyanoacrylate; GV, gastric varices; TIPS, transjugular intrahepatic portosystemic shunt; IVC, inferior vena cava.


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Gut and Liver

Vol.17 No.1
January, 2023

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